Login Register Cart 0
Generic placeholder image

Current Genomics

Editor-in-Chief

ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Lentiviral Transduction-based CRISPR/Cas9 Editing of Schistosoma mansoni Acetylcholinesterase

Author(s): Xiaofeng Du, Donald P. McManus, Juliet D. French, Haran Sivakumaran, Rebecca L. Johnston, Olga Kondrashova, Conor E. Fogarty, Malcolm K. Jones and Hong You*

Volume 24, Issue 3, 2023

Published on: 09 October, 2023

Page: [155 - 170] Pages: 16

DOI: 10.2174/1389202924666230823094608

open access plus

Abstract

Background: Recent studies on CRISPR/Cas9-mediated gene editing in Schistosoma mansoni have shed new light on the study and control of this parasitic helminth. However, the gene editing efficiency in this parasite is modest.

Methods: To improve the efficiency of CRISPR/Cas9 genome editing in schistosomes, we used lentivirus, which has been effectively used for gene editing in mammalian cells, to deliver plasmid DNA encoding Cas9 nuclease, a sgRNA targeting acetylcholinesterase (SmAChE) and a mCherry fluorescence marker into schistosomes.

Results: MCherry fluorescence was observed in transduced eggs, schistosomula, and adult worms, indicating that the CRISPR components had been delivered into these parasite stages by lentivirus. In addition, clearly changed phenotypes were observed in SmAChE-edited parasites, including decreased SmAChE activity, reduced hatching ability of edited eggs, and altered behavior of miracidia hatched from edited eggs. Next-generation sequencing analysis demonstrated that the lentiviral transductionbased CRISPR/Cas9 gene modifications in SmAChE-edited schistosomes were homology-directed repair predominant but with much lower efficiency than that obtained using electroporation (data previously published by our laboratory) for the delivery of CRISPR components.

Conclusion: Taken together, electroporation is more efficient than lentiviral transduction in the delivery of CRISPR/Cas9 into schistosomes for programmed genome editing. The exploration of tactics for enhancing CRISPR/Cas9 gene editing provides the basis for the future improvement of programmed genome editing in S. mansoni.

Keywords: Schistosoma mansoni, lentiviral transduction, CRISPR/Cas9, genome editing, acetylcholinesterase, efficiency.

« Previous Next »
Graphical Abstract

[1]
McManus, D.P.; Dunne, D.W.; Sacko, M.; Utzinger, J.; Vennervald, B.J.; Zhou, X.N. Schistosomiasis. Nat. Rev. Dis. Primers, 2018, 4(1), 13.
[http://dx.doi.org/10.1038/s41572-018-0013-8] [PMID: 30093684]
[2]
Gryseels, B.; Polman, K.; Clerinx, J.; Kestens, L. Human schistosomiasis. Lancet, 2006, 368(9541), 1106-1118.
[http://dx.doi.org/10.1016/S0140-6736(06)69440-3] [PMID: 16997665]
[3]
McManus, D.P.; Bergquist, R.; Cai, P.; Ranasinghe, S.; Tebeje, B.M.; You, H. Schistosomiasis—from immunopathology to vaccines. Semin. Immunopathol., 2020, 42(3), 355-371.
[http://dx.doi.org/10.1007/s00281-020-00789-x] [PMID: 32076812]
[4]
Deol, A.K.; Fleming, F.M.; Calvo-Urbano, B.; Walker, M.; Bucumi, V.; Gnandou, I.; Tukahebwa, E.M.; Jemu, S.; Mwingira, U.J.; Alkohlani, A.; Traoré, M.; Ruberanziza, E.; Touré, S.; Basáñez, M.G.; French, M.D.; Webster, J.P. Schistosomiasis—assessing progress toward the 2020 and 2025 global goals. N. Engl. J. Med., 2019, 381(26), 2519-2528.
[http://dx.doi.org/10.1056/NEJMoa1812165] [PMID: 31881138]
[5]
Zhou, Y.; Zheng, H.; Chen, X.; Zhang, L.; Wang, K.; Guo, J.; Huang, Z.; Zhang, B.; Huang, W.; Jin, K. The Schistosoma japonicum genome reveals features of host–parasite interplay. Nature, 2009, 460(7253), 345-351.
[http://dx.doi.org/10.1038/nature08140] [PMID: 19606140]
[6]
Luo, F.; Yin, M.; Mo, X.; Sun, C.; Wu, Q.; Zhu, B.; Xiang, M.; Wang, J.; Wang, Y.; Li, J.; Zhang, T.; Xu, B.; Zheng, H.; Feng, Z.; Hu, W. An improved genome assembly of the fluke Schistosoma japonicum. PLoS Negl. Trop. Dis., 2019, 13(8), e0007612.
[http://dx.doi.org/10.1371/journal.pntd.0007612] [PMID: 31390359]
[7]
Berriman, M.; Haas, B.J.; LoVerde, P.T.; Wilson, R.A.; Dillon, G.P.; Cerqueira, G.C.; Mashiyama, S.T.; Al-Lazikani, B.; Andrade, L.F.; Ashton, P.D.; Aslett, M.A.; Bartholomeu, D.C.; Blandin, G.; Caffrey, C.R.; Coghlan, A.; Coulson, R.; Day, T.A.; Delcher, A.; DeMarco, R.; Djikeng, A.; Eyre, T.; Gamble, J.A.; Ghedin, E.; Gu, Y.; Hertz-Fowler, C.; Hirai, H.; Hirai, Y.; Houston, R.; Ivens, A.; Johnston, D.A.; Lacerda, D.; Macedo, C.D.; McVeigh, P.; Ning, Z.; Oliveira, G.; Overington, J.P.; Parkhill, J.; Pertea, M.; Pierce, R.J.; Protasio, A.V.; Quail, M.A.; Rajandream, M.A.; Rogers, J.; Sajid, M.; Salzberg, S.L.; Stanke, M.; Tivey, A.R.; White, O.; Williams, D.L.; Wortman, J.; Wu, W.; Zamanian, M.; Zerlotini, A.; Fraser-Liggett, C.M.; Barrell, B.G.; El-Sayed, N.M. The genome of the blood fluke Schistosoma mansoni. Nature, 2009, 460(7253), 352-358.
[http://dx.doi.org/10.1038/nature08160] [PMID: 19606141]
[8]
Protasio, A.V.; Tsai, I.J.; Babbage, A.; Nichol, S.; Hunt, M.; Aslett, M.A.; De Silva, N.; Velarde, G.S.; Anderson, T.J.C.; Clark, R.C.; Davidson, C.; Dillon, G.P.; Holroyd, N.E.; LoVerde, P.T.; Lloyd, C.; McQuillan, J.; Oliveira, G.; Otto, T.D.; Parker-Manuel, S.J.; Quail, M.A.; Wilson, R.A.; Zerlotini, A.; Dunne, D.W.; Berriman, M. A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. PLoS Negl. Trop. Dis., 2012, 6(1), e1455.
[http://dx.doi.org/10.1371/journal.pntd.0001455] [PMID: 22253936]
[9]
Young, N.D.; Jex, A.R.; Li, B.; Liu, S.; Yang, L.; Xiong, Z.; Li, Y.; Cantacessi, C.; Hall, R.S.; Xu, X.; Chen, F.; Wu, X.; Zerlotini, A.; Oliveira, G.; Hofmann, A.; Zhang, G.; Fang, X.; Kang, Y.; Campbell, B.E.; Loukas, A.; Ranganathan, S.; Rollinson, D.; Rinaldi, G.; Brindley, P.J.; Yang, H.; Wang, J.; Wang, J.; Gasser, R.B. Whole-genome sequence of Schistosoma haematobium. Nat. Genet., 2012, 44(2), 221-225.
[http://dx.doi.org/10.1038/ng.1065] [PMID: 22246508]
[10]
Stroehlein, A.J.; Korhonen, P.K.; Chong, T.M.; Lim, Y.L.; Chan, K.G.; Webster, B.; Rollinson, D.; Brindley, P.J.; Gasser, R.B.; Young, N.D. High-quality Schistosoma haematobium genome achieved by single-molecule and long-range sequencing. Gigascience, 2019, 8(9), giz108.
[http://dx.doi.org/10.1093/gigascience/giz108] [PMID: 31494670]
[11]
Dalzell, J.J.; Warnock, N.D.; McVeigh, P.; Marks, N.J.; Mousley, A.; Atkinson, L.; Maule, A.G. Considering RNAi experimental design in parasitic helminths. Parasitology, 2012, 139(5), 589-604.
[http://dx.doi.org/10.1017/S0031182011001946] [PMID: 22216952]
[12]
Correnti, J.M.; Brindley, P.J.; Pearce, E.J. Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Mol. Biochem. Parasitol., 2005, 143(2), 209-215.
[http://dx.doi.org/10.1016/j.molbiopara.2005.06.007] [PMID: 16076506]
[13]
Fanelli, E.; Di Vito, M.; Jones, J.T.; De Giorgi, C. Analysis of chitin synthase function in a plant parasitic nematode, Meloidogyne artiellia, using RNAi. Gene, 2005, 349, 87-95.
[http://dx.doi.org/10.1016/j.gene.2004.11.045] [PMID: 15777697]
[14]
Rinaldi, G.; Morales, M.E.; Cancela, M.; Castillo, E.; Brindley, P.J.; Tort, J.F. Development of functional genomic tools in trematodes: RNA interference and luciferase reporter gene activity in Fasciola hepatica. PLoS Negl. Trop. Dis., 2008, 2(7), e260.
[http://dx.doi.org/10.1371/journal.pntd.0000260] [PMID: 18612418]
[15]
Vastenhouw, N.L.; Brunschwig, K.; Okihara, K.L.; Müller, F.; Tijsterman, M.; Plasterk, R.H.A. Long-term gene silencing by RNAi. Nature, 2006, 442(7105), 882-882.
[http://dx.doi.org/10.1038/442882a] [PMID: 16929289]
[16]
Cho, S.W.; Kim, S.; Kim, J.M.; Kim, J.S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol., 2013, 31(3), 230-232.
[http://dx.doi.org/10.1038/nbt.2507] [PMID: 23360966]
[17]
Cong, L.; Ran, F.A.; Cox, D.; Lin, S.; Barretto, R.; Habib, N.; Hsu, P.D.; Wu, X.; Jiang, W.; Marraffini, L.A.; Zhang, F. Multiplex genome engineering using CRISPR/Cas systems. Science, 2013, 339(6121), 819-823.
[http://dx.doi.org/10.1126/science.1231143] [PMID: 23287718]
[18]
Gratz, S.J.; Cummings, A.M.; Nguyen, J.N.; Hamm, D.C.; Donohue, L.K.; Harrison, M.M.; Wildonger, J.; O’Connor-Giles, K.M. Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics, 2013, 194(4), 1029-1035.
[http://dx.doi.org/10.1534/genetics.113.152710] [PMID: 23709638]
[19]
Mali, P.; Yang, L.; Esvelt, K.M.; Aach, J.; Guell, M.; DiCarlo, J.E.; Norville, J.E.; Church, G.M. RNA-guided human genome engineering via Cas9. Science, 2013, 339(6121), 823-826.
[http://dx.doi.org/10.1126/science.1232033] [PMID: 23287722]
[20]
Hwang, W.Y.; Fu, Y.; Reyon, D.; Maeder, M.L.; Tsai, S.Q.; Sander, J.D.; Peterson, R.T.; Yeh, J.R.J.; Joung, J.K. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol., 2013, 31(3), 227-229.
[http://dx.doi.org/10.1038/nbt.2501] [PMID: 23360964]
[21]
Friedland, A.E.; Tzur, Y.B.; Esvelt, K.M.; Colaiácovo, M.P.; Church, G.M.; Calarco, J.A. Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat. Methods, 2013, 10(8), 741-743.
[http://dx.doi.org/10.1038/nmeth.2532] [PMID: 23817069]
[22]
Bryant, J.M.; Baumgarten, S.; Glover, L.; Hutchinson, S.; Rachidi, N. CRISPR in parasitology: Not exactly cut and dried! Trends Parasitol., 2019, 35(6), 409-422.
[http://dx.doi.org/10.1016/j.pt.2019.03.004]
[23]
Castelletto, M.L.; Gang, S.S.; Hallem, E.A. Recent advances in functional genomics for parasitic nematodes of mammals. J. Exp. Biol.,, 2020, 223((Pt)(Suppl. 1)), jeb206482.
[http://dx.doi.org/10.1242/jeb.206482] [PMID: 32034038]
[24]
Gang, S.S.; Castelletto, M.L.; Bryant, A.S.; Yang, E.; Mancuso, N.; Lopez, J.B.; Pellegrini, M.; Hallem, E.A. Targeted mutagenesis in a human-parasitic nematode. PLoS Pathog., 2017, 13(10), e1006675.
[http://dx.doi.org/10.1371/journal.ppat.1006675] [PMID: 29016680]
[25]
Nakayama, K.; Ishita, Y.; Chihara, T.; Okumura, M. Screening for CRISPR/Cas9-induced mutations using a co-injection marker in the nematode Pristionchus pacificus. Dev. Genes Evol., 2020, 230(3), 257-264.
[http://dx.doi.org/10.1007/s00427-020-00651-y] [PMID: 32030512]
[26]
Ittiprasert, W.; Mann, V.H.; Karinshak, S.E.; Coghlan, A.; Rinaldi, G.; Sankaranarayanan, G.; Chaidee, A.; Tanno, T.; Kumkhaek, C.; Prangtaworn, P.; Mentink-Kane, M.M.; Cochran, C.J.; Driguez, P.; Holroyd, N.; Tracey, A.; Rodpai, R.; Everts, B.; Hokke, C.H.; Hoffmann, K.F.; Berriman, M.; Brindley, P.J. Programmed genome editing of the omega-1 ribonuclease of the blood fluke, Schistosoma mansoni. eLife, 2019, 8, e41337.
[http://dx.doi.org/10.7554/eLife.41337] [PMID: 30644357]
[27]
You, H.; Mayer, J.U.; Johnston, R.L.; Sivakumaran, H.; Ranasinghe, S.; Rivera, V.; Kondrashova, O.; Koufariotis, L.T.; Du, X.; Driguez, P.; French, J.D.; Waddell, N.; Duke, M.G.; Ittiprasert, W.; Mann, V.H.; Brindley, P.J.; Jones, M.K.; McManus, D.P. CRISPR/Cas9‐mediated genome editing of Schistosoma mansoni acetylcholinesterase. FASEB J., 2021, 35(1), e21205.
[http://dx.doi.org/10.1096/fj.202001745RR] [PMID: 33337558]
[28]
Sankaranarayanan, G.; Coghlan, A.; Driguez, P.; Lotkowska, M.E.; Sanders, M.; Holroyd, N.; Tracey, A.; Berriman, M.; Rinaldi, G. Large CRISPR-Cas-induced deletions in the oxamniquine resistance locus of the human parasite Schistosoma mansoni. Wellcome Open Res., 2020, 5, 178.
[http://dx.doi.org/10.12688/wellcomeopenres.16031.2] [PMID: 32789192]
[29]
Du, X.; McManus, D.P.; French, J.D.; Jones, M.K.; You, H. CRISPR/Cas9: A new tool for the study and control of helminth parasites. BioEssays, 2021, 43(1), 2000185.
[http://dx.doi.org/10.1002/bies.202000185] [PMID: 33145822]
[30]
Paix, A.; Folkmann, A.; Rasoloson, D.; Seydoux, G. High efficiency, homology-directed genome editing in Caenorhabditis elegans using CRISPR-Cas9 ribonucleoprotein complexes. Genetics, 2015, 201(1), 47-54.
[http://dx.doi.org/10.1534/genetics.115.179382] [PMID: 26187122]
[31]
Arribere, J.A.; Bell, R.T.; Fu, B.X.H.; Artiles, K.L.; Hartman, P.S.; Fire, A.Z. Efficient marker-free recovery of custom genetic modifications with CRISPR/Cas9 in Caenorhabditis elegans. Genetics, 2014, 198(3), 837-846.
[http://dx.doi.org/10.1534/genetics.114.169730] [PMID: 25161212]
[32]
Schwartz, M.L.; Davis, M.W.; Rich, M.S.; Jorgensen, E.M. High-efficiency CRISPR gene editing in C. elegans using Cas9 integrated into the genome. PLoS Genet., 2021, 17(11), e1009755.
[http://dx.doi.org/10.1371/journal.pgen.1009755] [PMID: 34748534]
[33]
Au, V.; Li-Leger, E.; Raymant, G.; Flibotte, S.; Chen, G.; Martin, K.; Fernando, L.; Doell, C.; Rosell, F.I.; Wang, S.; Edgley, M.L.; Rougvie, A.E.; Hutter, H.; Moerman, D.G. CRISPR/Cas9 methodology for the generation of knockout deletions in Caenorhabditis elegans. G3 , 2019, 9(1), 135-144.
[http://dx.doi.org/10.1534/g3.118.200778] [PMID: 30420468]
[34]
Huang, G.; de Jesus, B.; Koh, A.; Blanco, S.; Rettmann, A.; DeMott, E.; Sylvester, M.; Ren, C.; Meng, C.; Waterland, S. Improved CRISPR/Cas9 knock-in efficiency via the self-excising cassette (SEC) selection method in C. elegans; MicroPubl Biol, 2021.
[http://dx.doi.org/10.17912/micropub.biology.000460]
[35]
Wang, T.; Wei, J.J.; Sabatini, D.M.; Lander, E.S. Genetic screens in human cells using the CRISPR-Cas9 system. Science, 2014, 343(6166), 80-84.
[http://dx.doi.org/10.1126/science.1246981] [PMID: 24336569]
[36]
Cheong, T.C.; Compagno, M.; Chiarle, R. Editing of mouse and human immunoglobulin genes by CRISPR-Cas9 system. Nat. Commun., 2016, 7(1), 10934.
[http://dx.doi.org/10.1038/ncomms10934] [PMID: 26956543]
[37]
Min, Y.L.; Li, H.; Rodriguez-Caycedo, C.; Mireault, A.A.; Huang, J.; Shelton, J.M.; McAnally, J.R.; Amoasii, L.; Mammen, P.P.A.; Bassel-Duby, R.; Olson, E.N. CRISPR-Cas9 corrects Duchenne muscular dystrophy exon 44 deletion mutations in mice and human cells. Sci. Adv., 2019, 5(3), eaav4324.
[http://dx.doi.org/10.1126/sciadv.aav4324] [PMID: 30854433]
[38]
Ramakrishna, S.; Kwaku Dad, A.B.; Beloor, J.; Gopalappa, R.; Lee, S.K.; Kim, H. Gene disruption by cell-penetrating peptide-mediated delivery of Cas9 protein and guide RNA. Genome Res., 2014, 24(6), 1020-1027.
[http://dx.doi.org/10.1101/gr.171264.113] [PMID: 24696462]
[39]
Banan, M. Recent advances in CRISPR/Cas9-mediated knock-ins in mammalian cells. J. Biotechnol., 2020, 308, 1-9.
[http://dx.doi.org/10.1016/j.jbiotec.2019.11.010] [PMID: 31751596]
[40]
Ghorbal, M.; Gorman, M.; Macpherson, C.R.; Martins, R.M.; Scherf, A.; Lopez-Rubio, J.J. Genome editing in the human malaria parasite Plasmodium falciparum using the CRISPR-Cas9 system. Nat. Biotechnol., 2014, 32(8), 819-821.
[http://dx.doi.org/10.1038/nbt.2925] [PMID: 24880488]
[41]
Knuepfer, E.; Napiorkowska, M.; van Ooij, C.; Holder, A.A. Generating conditional gene knockouts in Plasmodium – a toolkit to produce stable DiCre recombinase-expressing parasite lines using CRISPR/Cas9. Sci. Rep., 2017, 7(1), 3881.
[http://dx.doi.org/10.1038/s41598-017-03984-3] [PMID: 28634346]
[42]
Soares Medeiros, L.C.; South, L.; Peng, D.; Bustamante, J.M.; Wang, W.; Bunkofske, M.; Perumal, N.; Sanchez-Valdez, F.; Tarleton, R.L. Rapid, selection-free, high-efficiency genome editing in protozoan parasites using CRISPR-Cas9 ribonucleoproteins. MBio, 2017, 8(6), e01788-e17.
[http://dx.doi.org/10.1128/mBio.01788-17] [PMID: 29114029]
[43]
Janssen, B.D.; Chen, Y.P.; Molgora, B.M.; Wang, S.E.; Simoes-Barbosa, A.; Johnson, P.J. CRISPR/Cas9-mediated gene modification and gene knock out in the human-infective parasite Trichomonas vaginalis. Sci. Rep., 2018, 8(1), 270.
[http://dx.doi.org/10.1038/s41598-017-18442-3] [PMID: 29321601]
[44]
Lee, M.C.S.; Lindner, S.E.; Lopez-Rubio, J.J.; Llinás, M. Cutting back malaria: CRISPR/Cas9 genome editing of Plasmodium. Brief. Funct. Genomics, 2019, 18(5), 281-289.
[http://dx.doi.org/10.1093/bfgp/elz012] [PMID: 31365053]
[45]
Boltryk, S.D.; Passecker, A.; Alder, A.; Carrington, E.; van de Vegte-Bolmer, M.; van Gemert, G.J.; van der Starre, A.; Beck, H.P.; Sauerwein, R.W.; Kooij, T.W.A.; Brancucci, N.M.B.; Proellochs, N.I.; Gilberger, T.W.; Voss, T.S. CRISPR/Cas9-engineered inducible gametocyte producer lines as a valuable tool for Plasmodium falciparum malaria transmission research. Nat. Commun., 2021, 12(1), 4806.
[http://dx.doi.org/10.1038/s41467-021-24954-4] [PMID: 34376675]
[46]
Lino, C.A.; Harper, J.C.; Carney, J.P.; Timlin, J.A. Delivering CRISPR: A review of the challenges and approaches. Drug Deliv., 2018, 25(1), 1234-1257.
[http://dx.doi.org/10.1080/10717544.2018.1474964] [PMID: 29801422]
[47]
Cao, F.; Xie, X.; Gollan, T.; Zhao, L.; Narsinh, K.; Lee, R.J.; Wu, J.C. Comparison of gene-transfer efficiency in human embryonic stem cells. Mol. Imaging Biol., 2010, 12(1), 15-24.
[http://dx.doi.org/10.1007/s11307-009-0236-x] [PMID: 19551446]
[48]
Elegheert, J.; Behiels, E.; Bishop, B.; Scott, S.; Woolley, R.E.; Griffiths, S.C.; Byrne, E.F.X.; Chang, V.T.; Stuart, D.I.; Jones, E.Y.; Siebold, C.; Aricescu, A.R. Lentiviral transduction of mammalian cells for fast, scalable and high-level production of soluble and membrane proteins. Nat. Protoc., 2018, 13(12), 2991-3017.
[http://dx.doi.org/10.1038/s41596-018-0075-9] [PMID: 30455477]
[49]
You, H.; Liu, C.; Du, X.; McManus, D.P. Acetylcholinesterase and nicotinic acetylcholine receptors in schistosomes and other parasitic helminths. Molecules, 2017, 22(9), 1550.
[http://dx.doi.org/10.3390/molecules22091550]
[50]
Bueding, E. Acetylcholinesterase activity of Schistosoma mansoni. Br. J. Pharmacol. Chemother., 1952, 7(4), 563-566.
[http://dx.doi.org/10.1111/j.1476-5381.1952.tb00722.x] [PMID: 13019023]
[51]
Barker, L.R.; Bueding, E.; Timms, A. The possible role of acetylcholine in Schistosoma mansoni. Br. J. Pharmacol. Chemother., 1966, 26(3), 656-665.
[http://dx.doi.org/10.1111/j.1476-5381.1966.tb01845.x]
[52]
Jones, A.K.; Bentley, G.N.; Parra, W.G.O.; Agnew, A. Molecular characterization of an acetylcholinesterase implicated in the regulation of glucose scavenging by the parasite Schistosoma. FASEB J., 2002, 16(3), 441-443.
[http://dx.doi.org/10.1096/fj.01-0683fje] [PMID: 11821256]
[53]
You, H.; Liu, C.; Du, X.; Nawaratna, S.; Rivera, V.; Harvie, M.; Jones, M.; McManus, D. Suppression of Schistosoma japonicum acetylcholinesterase affects parasite growth and development. Int. J. Mol. Sci., 2018, 19(8), 2426.
[http://dx.doi.org/10.3390/ijms19082426] [PMID: 30115897]
[54]
You, H.; Gobert, G.N.; Du, X.; Pali, G.; Cai, P.; Jones, M.K.; McManus, D.P. Functional characterisation of Schistosoma japonicum acetylcholinesterase. Parasit. Vectors, 2016, 9(1), 328.
[http://dx.doi.org/10.1186/s13071-016-1615-1] [PMID: 27283196]
[55]
Dalton, J.P.; Day, S.R.; Drew, A.C.; Brindley, P.J. A method for the isolation of schistosome eggs and miracidia free of contaminating host tissues. Parasitology, 1997, 115(1), 29-32.
[http://dx.doi.org/10.1017/S0031182097001091] [PMID: 9226954]
[56]
Ashton, P.D.; Harrop, R.; Shah, B.; Wilson, R.A. The schistosome egg: Development and secretions. Parasitology, 2001, 122(3), 329-338.
[http://dx.doi.org/10.1017/S0031182001007351] [PMID: 11289069]
[57]
Du, X.; Jones, M.; Nawaratna, S.; Ranasinghe, S.; Xiong, C.; Cai, P.; McManus, D.; You, H. Gene expression in developmental stages of Schistosoma japonicum provides further insight into the importance of the Schistosome insulin-like peptide. Int. J. Mol. Sci., 2019, 20(7), 1565.
[http://dx.doi.org/10.3390/ijms20071565] [PMID: 30925781]
[58]
Milligan, J.N.; Jolly, E.R. Cercarial transformation and in vitro cultivation of Schistosoma mansoni schistosomules. J. Vis. Exp., 2011, (54), 3191.
[http://dx.doi.org/10.3791/3191-v] [PMID: 21876520]
[59]
Oliveros, J.C.; Franch, M.; Tabas-Madrid, D.; San-León, D.; Montoliu, L.; Cubas, P.; Pazos, F. Breaking-Cas—interactive design of guide RNAs for CRISPR-Cas experiments for ENSEMBL genomes. Nucleic Acids Res., 2016, 44(W1), W267-W271.
[http://dx.doi.org/10.1093/nar/gkw407] [PMID: 27166368]
[60]
Ran, F.A.; Hsu, P.D.; Wright, J.; Agarwala, V.; Scott, D.A.; Zhang, F. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc., 2013, 8(11), 2281-2308.
[http://dx.doi.org/10.1038/nprot.2013.143] [PMID: 24157548]
[61]
Yoo, S.; Mittelstein, D.R.; Hurt, R.C.; Lacroix, J.; Shapiro, M.G. Focused ultrasound excites cortical neurons via mechanosensitive calcium accumulation and ion channel amplification. Nat. Commun., 2022, 13(1), 493.
[http://dx.doi.org/10.1038/s41467-022-28040-1] [PMID: 35078979]
[62]
Mann, V.H.; Suttiprapa, S.; Rinaldi, G.; Brindley, P.J. Establishing transgenic schistosomes. PLoS Negl. Trop. Dis., 2011, 5(8), e1230.
[http://dx.doi.org/10.1371/journal.pntd.0001230] [PMID: 21912709]
[63]
Jurberg, A.D.; Gonçalves, T.; Costa, T.A.; de Mattos, A.C.A.; Pascarelli, B.M.; de Manso, P.P.A.; Ribeiro-Alves, M.; Pelajo-Machado, M.; Peralta, J.M.; Coelho, P.M.Z.; Lenzi, H.L. The embryonic development of Schistosoma mansoni eggs: Proposal for a new staging system. Dev. Genes Evol., 2009, 219(5), 219-234.
[http://dx.doi.org/10.1007/s00427-009-0285-9] [PMID: 19415326]
[64]
Zheng, X.; Hu, X.; Zhou, G.; Lu, Z.; Qiu, W.; Bao, J.; Dai, Y. Soluble egg antigen from Schistosoma japonicum modulates the progression of chronic progressive experimental autoimmune encephalomyelitis via Th2-shift response. J. Neuroimmunol., 2008, 194(1-2), 107-114.
[http://dx.doi.org/10.1016/j.jneuroim.2007.12.001] [PMID: 18207251]
[65]
Du, X.; McManus, D.P.; Cai, P.; Hu, W.; You, H. Identification and functional characterisation of a Schistosoma japonicum insulin-like peptide. Parasit. Vectors, 2017, 10(1), 181.
[http://dx.doi.org/10.1186/s13071-017-2095-7] [PMID: 28407789]
[66]
Du, X.; McManus, D.P.; Fogarty, C.E.; Jones, M.K.; You, H. Schistosoma mansoni fibroblast growth factor receptor a orchestrates multiple functions in schistosome biology and in the host-parasite interplay. Front. Immunol., 2022, 13, 868077.
[http://dx.doi.org/10.3389/fimmu.2022.868077] [PMID: 35812433]
[67]
Wang, T.; Wyeth, R.C.; Liang, D.; Bose, U.; Ni, G.; McManus, D.P.; Cummins, S.F. A Biomphalaria glabrata peptide that stimulates significant behaviour modifications in aquatic free-living Schistosoma mansoni miracidia. PLoS Negl. Trop. Dis., 2019, 13(1), e0006948.
[http://dx.doi.org/10.1371/journal.pntd.0006948] [PMID: 30668561]
[68]
Wyeth, R.C.; Braubach, O.R.; Fine, A.; Croll, R.P. Videograms: A method for repeatable unbiased quantitative behavioral analysis without scoring or tracking.In: Zebrafish neurobehavioral protocols; Springer, 2011, pp. 15-33.
[http://dx.doi.org/10.1007/978-1-60761-953-6_2]
[69]
Fogarty, C.E.; Zhao, M.; McManus, D.P.; Duke, M.G.; Cummins, S.F.; Wang, T. Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata. Parasit. Vectors, 2019, 12(1), 452.
[http://dx.doi.org/10.1186/s13071-019-3708-0] [PMID: 31521183]
[70]
Shah, A.N.; Davey, C.F.; Whitebirch, A.C.; Miller, A.C.; Moens, C.B. Rapid reverse genetic screening using CRISPR in zebrafish. Nat. Methods, 2015, 12(6), 535-540.
[http://dx.doi.org/10.1038/nmeth.3360] [PMID: 25867848]
[71]
Li, B.; Ren, N.; Yang, L.; Liu, J.; Huang, Q. A qPCR method for genome editing efficiency determination and single-cell clone screening in human cells. Sci. Rep., 2019, 9(1), 18877.
[http://dx.doi.org/10.1038/s41598-019-55463-6] [PMID: 31827197]
[72]
Clement, K.; Rees, H.; Canver, M.C.; Gehrke, J.M.; Farouni, R.; Hsu, J.Y.; Cole, M.A.; Liu, D.R.; Joung, J.K.; Bauer, D.E.; Pinello, L. CRISPResso2 provides accurate and rapid genome editing sequence analysis. Nat. Biotechnol., 2019, 37(3), 224-226.
[http://dx.doi.org/10.1038/s41587-019-0032-3] [PMID: 30809026]
[73]
Jia, H.; Guo, Y.; Zhao, W.; Wang, K. Long-range PCR in next-generation sequencing: Comparison of six enzymes and evaluation on the MiSeq sequencer. Sci. Rep., 2014, 4(1), 5737.
[http://dx.doi.org/10.1038/srep05737] [PMID: 25034901]
[74]
Walczak, M.; Skrzypczak-Zielinska, M.; Plucinska, M.; Zakerska-Banaszak, O.; Marszalek, D.; Lykowska-Szuber, L.; Stawczyk-Eder, K.; Dobrowolska, A.; Slomski, R. Long-range PCR libraries and next-generation sequencing for pharmacogenetic studies of patients treated with anti-TNF drugs. Pharmacogenomics J., 2019, 19(4), 358-367.
[http://dx.doi.org/10.1038/s41397-018-0058-9] [PMID: 30293984]
[75]
Zhao, P.; Zhang, Z.; Ke, H.; Yue, Y.; Xue, D. Oligonucleotide-based targeted gene editing in C. elegans via the CRISPR/Cas9 system. Cell Res., 2014, 24(2), 247-250.
[http://dx.doi.org/10.1038/cr.2014.9] [PMID: 24418757]
[76]
Paix, A.; Wang, Y.; Smith, H.E.; Lee, C.Y.S.; Calidas, D.; Lu, T.; Smith, J.; Schmidt, H.; Krause, M.W.; Seydoux, G. Scalable and versatile genome editing using linear DNAs with microhomology to Cas9 Sites in Caenorhabditis elegans. Genetics, 2014, 198(4), 1347-1356.
[http://dx.doi.org/10.1534/genetics.114.170423] [PMID: 25249454]
[77]
Ward, J.D. Rapid and precise engineering of the Caenorhabditis elegans genome with lethal mutation co-conversion and inactivation of NHEJ repair. Genetics, 2015, 199(2), 363-377.
[http://dx.doi.org/10.1534/genetics.114.172361] [PMID: 25491644]
[78]
Zhang, W.W.; Lypaczewski, P.; Matlashewski, G. Optimized CRISPR-Cas9 genome editing for Leishmania and its use to target a multigene family, induce chromosomal translocation, and study DNA break repair mechanisms. MSphere, 2017, 2(1), e00340-e16.
[http://dx.doi.org/10.1128/mSphere.00340-16] [PMID: 28124028]
[79]
Chen, C.; Fenk, L.A.; de Bono, M. Efficient genome editing in Caenorhabditis elegans by CRISPR-targeted homologous recombination. Nucleic Acids Res., 2013, 41(20), e193-e193.
[http://dx.doi.org/10.1093/nar/gkt805] [PMID: 24013562]
[80]
Clarke, R.; Heler, R.; MacDougall, M.S.; Yeo, N.C.; Chavez, A.; Regan, M.; Hanakahi, L.; Church, G.M.; Marraffini, L.A.; Merrill, B.J. Enhanced bacterial immunity and mammalian genome editing via rna-polymerase-mediated dislodging of Cas9 from double-strand DNA breaks. Mol. Cell, 2018, 71(1), 42-55.e8.
[http://dx.doi.org/10.1016/j.molcel.2018.06.005]
[81]
Ortinski, P.I.; O’Donovan, B.; Dong, X.; Kantor, B. Integrase-deficient lentiviral vector as an all-in-one platform for highly efficient CRISPR/Cas9-mediated gene editing. Mol. Ther. Methods Clin. Dev., 2017, 5, 153-164.
[http://dx.doi.org/10.1016/j.omtm.2017.04.002] [PMID: 28497073]
[82]
Petris, G.; Casini, A.; Montagna, C.; Lorenzin, F.; Prandi, D.; Romanel, A.; Zasso, J.; Conti, L.; Demichelis, F.; Cereseto, A. Hit and go CAS9 delivered through a lentiviral based self-limiting circuit. Nat. Commun., 2017, 8(1), 15334.
[http://dx.doi.org/10.1038/ncomms15334] [PMID: 28530235]
[83]
Adams, S.; Pathak, P.; Shao, H.; Lok, J.B.; Pires-daSilva, A. Liposome-based transfection enhances RNAi and CRISPR-mediated mutagenesis in non-model nematode systems. Sci. Rep., 2019, 9(1), 483.
[http://dx.doi.org/10.1038/s41598-018-37036-1] [PMID: 30679624]
[84]
Suresh, B.; Ramakrishna, S.; Kim, H. Cell-penetrating peptide-mediated delivery of Cas9 protein and guide RNA for genome editing.In: Eukaryotic Transcriptional and Post-Transcriptional Gene Expression Regulation; Springer, 2017, pp. 81-94.
[http://dx.doi.org/10.1007/978-1-4939-6518-2_7]
[85]
Geng, J.; Xia, X.; Teng, L.; Wang, L.; Chen, L.; Guo, X.; Belingon, B.; Li, J.; Feng, X.; Li, X.; Shang, W.; Wan, Y.; Wang, H. Emerging landscape of cell-penetrating peptide-mediated nucleic acid delivery and their utility in imaging, gene-editing, and RNA-sequencing. J. Control. Release, 2022, 341, 166-183.
[http://dx.doi.org/10.1016/j.jconrel.2021.11.032] [PMID: 34822907]
[86]
Finn, J.D.; Smith, A.R.; Patel, M.C.; Shaw, L.; Youniss, M.R.; van Heteren, J.; Dirstine, T.; Ciullo, C.; Lescarbeau, R.; Seitzer, J.; Shah, R.R.; Shah, A.; Ling, D.; Growe, J.; Pink, M.; Rohde, E.; Wood, K.M.; Salomon, W.E.; Harrington, W.F.; Dombrowski, C.; Strapps, W.R.; Chang, Y.; Morrissey, D.V. A single administration of CRISPR/Cas9 lipid nanoparticles achieves robust and persistent in vivo genome editing. Cell Rep., 2018, 22(9), 2227-2235.
[http://dx.doi.org/10.1016/j.celrep.2018.02.014] [PMID: 29490262]
[87]
Qiu, M.; Li, Y.; Bloomer, H.; Xu, Q. Developing biodegradable lipid nanoparticles for intracellular mRNA delivery and genome editing. Acc. Chem. Res., 2021, 54(21), 4001-4011.
[http://dx.doi.org/10.1021/acs.accounts.1c00500] [PMID: 34668716]
[88]
Han, J.P.; Kim, M.; Choi, B.S.; Lee, J.H.; Lee, G.S.; Jeong, M.; Lee, Y.; Kim, E.A.; Oh, H.K.; Go, N.; Lee, H.; Lee, K.J.; Kim, U.G.; Lee, J.Y.; Kim, S.; Chang, J.; Lee, H.; Song, D.W.; Yeom, S.C. In vivo delivery of CRISPR-Cas9 using lipid nanoparticles enables antithrombin gene editing for sustainable hemophilia A and B therapy. Sci. Adv., 2022, 8(3), eabj6901.
[http://dx.doi.org/10.1126/sciadv.abj6901] [PMID: 35061543]
[89]
Junio, A.B.; Li, X.; Massey, H.C., Jr; Nolan, T.J.; Todd Lamitina, S.; Sundaram, M.V.; Lok, J.B. Strongyloides stercoralis: Cell- and tissue-specific transgene expression and co-transformation with vector constructs incorporating a common multifunctional 3′ UTR. Exp. Parasitol., 2008, 118(2), 253-265.
[http://dx.doi.org/10.1016/j.exppara.2007.08.018] [PMID: 17945217]
[90]
Song, J.; Yang, D.; Xu, J.; Zhu, T.; Chen, Y.E.; Zhang, J. RS-1 enhances CRISPR/Cas9- and TALEN-mediated knock-in efficiency. Nat. Commun., 2016, 7(1), 10548.
[http://dx.doi.org/10.1038/ncomms10548] [PMID: 26817820]
[91]
Lamas-Toranzo, I.; Martínez-Moro, A.; O’Callaghan, E.; Millán-Blanca, G.; Sánchez, J.M.; Lonergan, P.; Bermejo-Álvarez, P. RS‐1 enhances CRISPR‐mediated targeted knock‐in in bovine embryos. Mol. Reprod. Dev., 2020, 87(5), 542-549.
[http://dx.doi.org/10.1002/mrd.23341] [PMID: 32227559]
[92]
Ding, X.; Seebeck, T.; Feng, Y.; Jiang, Y.; Davis, G.D.; Chen, F. Improving CRISPR-Cas9 genome editing efficiency by fusion with chromatin-modulating peptides. CRISPR J., 2019, 2(1), 51-63.
[http://dx.doi.org/10.1089/crispr.2018.0036] [PMID: 31021236]
[93]
Mitsunobu, H.; Teramoto, J.; Nishida, K.; Kondo, A. Beyond native Cas9: manipulating genomic information and function. Trends Biotechnol., 2017, 35(10), 983-996.
[http://dx.doi.org/10.1016/j.tibtech.2017.06.004] [PMID: 28739220]
[94]
Najm, F.J.; Strand, C.; Donovan, K.F.; Hegde, M.; Sanson, K.R.; Vaimberg, E.W.; Sullender, M.E.; Hartenian, E.; Kalani, Z.; Fusi, N.; Listgarten, J.; Younger, S.T.; Bernstein, B.E.; Root, D.E.; Doench, J.G. Orthologous CRISPR–Cas9 enzymes for combinatorial genetic screens. Nat. Biotechnol., 2018, 36(2), 179-189.
[http://dx.doi.org/10.1038/nbt.4048] [PMID: 29251726]
[95]
Gasiunas, G.; Young, J.K.; Karvelis, T.; Kazlauskas, D.; Urbaitis, T.; Jasnauskaite, M.; Grusyte, M.M.; Paulraj, S.; Wang, P.H.; Hou, Z.; Dooley, S.K.; Cigan, M.; Alarcon, C.; Chilcoat, N.D.; Bigelyte, G.; Curcuru, J.L.; Mabuchi, M.; Sun, Z.; Fuchs, R.T.; Schildkraut, E.; Weigele, P.R.; Jack, W.E.; Robb, G.B.; Venclovas, Č.; Siksnys, V. A catalogue of biochemically diverse CRISPR-Cas9 orthologs. Nat. Commun., 2020, 11(1), 5512.
[http://dx.doi.org/10.1038/s41467-020-19344-1] [PMID: 33139742]
[96]
Yang, H.; Patel, D.J.; Cas, X. A new and small CRISPR gene-editing protein. Cell Res., 2019, 29(5), 345-346.
[http://dx.doi.org/10.1038/s41422-019-0165-4] [PMID: 30992542]
[97]
Yang, Z.; Edwards, H.; Xu, P. CRISPR-Cas12a/Cpf1-assisted precise, efficient and multiplexed genome-editing in Yarrowia lipolytica. Metab. Eng. Commun., 2020, 10, e00112.
[http://dx.doi.org/10.1016/j.mec.2019.e00112] [PMID: 31867213]
[98]
Ittiprasert, W.; Chatupheeraphat, C.; Mann, V.H.; Li, W.; Miller, A.; Ogunbayo, T.; Tran, K.; Alrefaei, Y.N.; Mentink-Kane, M.; Brindley, P.J. RNA-guided As Cas12a-and Sp Cas9-catalyzed knockout and homology directed repair of the omega-1 locus of the human blood fluke, Schistosoma mansoni. Int. J. Mol. Sci., 2022, 23(2), 631.
[http://dx.doi.org/10.3390/ijms23020631] [PMID: 35054816]
[99]
Zhang, S.; Shen, J.; Li, D.; Cheng, Y. Strategies in the delivery of Cas9 ribonucleoprotein for CRISPR/Cas9 genome editing. Theranostics, 2021, 11(2), 614-648.
[http://dx.doi.org/10.7150/thno.47007] [PMID: 33391496]
[100]
You, H.; Jones, M.K.; Whitworth, D.J.; McManus, D.P. Innovations and advances in schistosome stem cell research. Front. Immunol., 2021, 12, 599014.
[http://dx.doi.org/10.3389/fimmu.2021.599014] [PMID: 33746946]

Rights & Permissions Print Cite
Article Metrics
22
2
© 2024 Bentham Science Publishers | Privacy Policy