Advances in the Genetic Manipulation of Nosema bombycis.
Genetic manipulation
In vitro cell culture systems
Nosema bombycis
RNAi
Silkworm pathogens
Sporoplasm
Transfection
Journal
Experientia supplementum (2012)
ISSN: 1664-431X
Titre abrégé: Exp Suppl
Pays: Switzerland
ID NLM: 101738007
Informations de publication
Date de publication:
2022
2022
Historique:
entrez:
11
5
2022
pubmed:
12
5
2022
medline:
17
5
2022
Statut:
ppublish
Résumé
The microsporidium Nosema bombycis can infect and transmit both vertically and horizontally in multiple lepidopteran insects including silkworms and crop pests. While there have been several studies on the N. bombycis spore, there have been only limited studies on the N. bombycis sporoplasm. This chapter reviews what is known about this life cycle stage as well as published studies on purification of the N. bombycis sporoplasm and its survival in an in vitro cell culture system. Genetic transformation techniques have revolutionized the study of many pathogenic organisms. While progress has been made on the development of such systems for microsporidia, this critical problem has not been solved for these pathogens. This chapter provides a summary of the latest research progress on genetic manipulation of N. bombycis.
Identifiants
pubmed: 35544002
doi: 10.1007/978-3-030-93306-7_6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
137-152Informations de copyright
© 2022. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Avery SW, Anthony DW (1983) Ultrastructural study of early development of Nosema algerae in Anopheles albimanus. J Invertebr Pathol 42(1):87–95
doi: 10.1016/0022-2011(83)90206-9
Balu B, Shoue DA, Fraser MJ Jr, Adams JH (2005) High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Proc Natl Acad Sci U S A 102(45):16391–16396. https://doi.org/10.1073/pnas.0504679102 . PubMed PMID: 16260745; PubMed Central PMCID: PMCPMC1275597
doi: 10.1073/pnas.0504679102
pubmed: 16260745
pmcid: 1275597
Black M, Seeber F, Soldati D, Kim K, Boothroyd JC (1995) Restriction enzyme-mediated integration elevates transformation frequency and enables co-transfection of Toxoplasma gondii. Mol Biochem Parasit 74(1):55–63. https://doi.org/10.1016/0166-6851(95)02483-2 . PMID: 8719245
doi: 10.1016/0166-6851(95)02483-2
Cali A, Weiss LM, Takvorian PM (2002) Brachiola algerae spore membrane systems, their activity during extrusion, and a new structural entity, the multilayered interlaced network, associated with the polar tube and the sporoplasm. J Eukaryot Microbiol 49(2):164–174
doi: 10.1111/j.1550-7408.2002.tb00361.x
Chen HM, Guo YJ, Qiu YS, Huang HB, Lin CQ, Liu M, Chen X, Yang P, Wu K (2019) Efficient genome engineering of Toxoplasma gondii using the TALEN technique. Parasite Vector. 12:112. https://doi.org/10.1186/s13071-019-3378-y . PMID: 30876436 PMCID: PMC6419828
doi: 10.1186/s13071-019-3378-y
Choudhary HH, Nava MG, Gartlan BE, Rose S, Vinayak S (2020) A conditional protein degradation system to study essential gene function in Cryptosporidium parvum. MBio 11(4):e01231–e01220. https://doi.org/10.1128/mBio.01231-20 . PubMed PMID: 32843543; PubMed Central PMCID: PMCPMC7448269
doi: 10.1128/mBio.01231-20
pubmed: 32843543
pmcid: 7448269
Donald RGK, Roos DS (1993) Stable molecular-transformation of Toxoplasma gondii - a selectable dihydrofolate reductase-thymidylate synthase marker based on drug-resistance mutations in malaria. P Natl Acad Sci USA. 90(24):11703–11707. https://doi.org/10.1073/pnas.90.24.11703 . PMID: 8265612 PMCID: PMC48052
doi: 10.1073/pnas.90.24.11703
Fonager J, Franke-Fayard BM, Adams JH, Ramesar J, Klop O, Khan SM, Janse CJ, Waters AP (2011) Development of the piggyBac transposable system for Plasmodium berghei and its application for random mutagenesis in malaria parasites. BMC Genomics 12:155. https://doi.org/10.1186/1471-2164-12-155 . PMID: 21418605 PMCID: PMC3073922
doi: 10.1186/1471-2164-12-155
pubmed: 21418605
pmcid: 3073922
Ghorbal M, Gorman M, Macpherson CR, Martins RM, Scherf A, Lopez-Rubio JJ (2014) Genome editing in the human malaria parasite Plasmodium falciparum using the CRISPR-Cas9 system. Nat Biotechnol 32(8):819–821. https://doi.org/10.1038/nbt.2925
doi: 10.1038/nbt.2925
pubmed: 24880488
Goonewardene R, Daily J, Kaslow D, Sullivan TJ, Duffy P, Carter R et al (1993) Transfection of the malaria parasite and expression of firefly luciferase. Proc Natl Acad Sci U S A 90(11):5234–5236. https://doi.org/10.1073/pnas.90.11.5234 . Epub 1993/06/01. PubMed PMID: 8506371; PubMed Central PMCID: PMCPMC46690
doi: 10.1073/pnas.90.11.5234
pubmed: 8506371
pmcid: 46690
Guo R, Cao GL, Lu YH, Xue RY, Kumar D, Hu XL, Gong C (2016) Exogenous gene can be integrated into Nosema bombycis genome by mediating with a non-transposon vector. Parasitol Res 115(8):3093–3098. PubMed PMID: PMID: 27083186
doi: 10.1007/s00436-016-5064-8
He Q, Vossbrinck CR, Yang Q, Meng XZ, Luo J, Pan GQ, Zhou Z-Y, Li T (2019) Evolutionary and functional studies on microsporidian ATP-binding cassettes: insights into the adaptation of microsporidia to obligated intracellular parasitism. Infect Genet Evol 68:136–144. https://doi.org/10.1016/j.meegid.2018.12.022 . PMID: 30576836
doi: 10.1016/j.meegid.2018.12.022
pubmed: 30576836
He Q, Luo J, Xu JZ, Wang CX, Meng XZ, Pan GQ et al (2020a) Morphology and Transcriptome analysis of Nosema bombycis sporoplasm and insights into the initial infection of microsporidia. mSphere 5(1):e00958-19. https://doi.org/10.1128/mSphere.00958-19 . Epub 2020/02/14. PubMed PMID: 32051240; PubMed Central PMCID: PMCPMC7021473
doi: 10.1128/mSphere.00958-19
pubmed: 32051240
pmcid: 7021473
He Q, Luo J, Xu JZ, Meng XZ, Pan GQ, Li T, Zhou Z-Y (2020b) In-vitro cultivation of Nosema bombycis sporoplasms: a method for potential genetic engineering of microsporidia. J Invertebr Pathol 174:107420. Epub 2020/06/12. https://doi.org/10.1016/j.jip.2020.107420
doi: 10.1016/j.jip.2020.107420
pubmed: 32522660
He Q, Luo J, Xu JZ, Meng XZ, Pan GQ, Li T (2020c) Zhou Z-Y characterization of Hsp70 gene family provides insight into its functions related to microsporidian proliferation. J Invertebr Pathol 174:107394. https://doi.org/10.1016/j.jip.2020.107394 . PMID: 32428446
doi: 10.1016/j.jip.2020.107394
pubmed: 32428446
Heinz E, Williams TA, Nakjang S, Noel CJ, Swan DC, Goldberg AV, Harris SR, Weinmaier T, Markert S, Becher D, Bernhardt J, Dagan T, Hacker C, Lucocq JM, Schweder T, Rattei T, Hall N, Hirt RP, Embley TM (2012) The genome of the obligate intracellular parasite Trachipleistophora hominis: New insights into microsporidian genome dynamics and reductive evolution. PloS Pathogens 8(10):e1002979. https://doi.org/10.1371/journal.ppat.1002979 . PMID: 23133373 PMCID: PMC3486916
doi: 10.1371/journal.ppat.1002979
pubmed: 23133373
pmcid: 3486916
Huang Y, Zheng S, Mei X, Yu B, Sun B, Li B, Wei J, Chen J, Li T, Pan G, Zhou Z, Li C (2018) A secretory hexokinase plays an active role in the proliferation of Nosema bombycis. PeerJ. 6:e5658. https://doi.org/10.7717/peerj.5658 . PMID: 30258733 PMCID: PMC6152459
doi: 10.7717/peerj.5658
pubmed: 30258733
pmcid: 6152459
Ishihara R, Hayashi Y (1968) Some properties of ribosomes from the sporoplasm of Nosema bombycis. J Invertebr Pathol 11(3):377–385
doi: 10.1016/0022-2011(68)90186-9
Kim K, Soldati D, Boothroyd JC (1993) Gene replacement in Toxoplasma gondii with chloramphenicol acetyltransferase as selectable marker. Science 262(5135):911–914. https://doi.org/10.1126/science.8235614 . PMID: 8235614
doi: 10.1126/science.8235614
pubmed: 8235614
Li W, Evans JD, Huang Q, Rodriguez-Garcia C, Liu J, Hamilton M, Grozinger CM, Webster TC, Su S, Chen YP (2016) Silencing the honey bee (Apis mellifera) naked cuticle gene (nkd) improves host immune function and reduces Nosema ceranae infections. Appl Environ Microbiol 82(22):6779–6787. https://doi.org/10.1128/AEM.02105-16 . PMID: 27613683 PMCID: PMC5086571
doi: 10.1128/AEM.02105-16
pubmed: 27613683
pmcid: 5086571
Mohring F, Hart MN, Rawlinson TA, Henrici R, Charleston JA, Diez Benavente E et al (2019) Rapid and iterative genome editing in the malaria parasite Plasmodium knowlesi provides new tools for P. vivax research. elife 8:e45829. https://doi.org/10.7554/eLife.45829
doi: 10.7554/eLife.45829
pubmed: 31205002
pmcid: 6579517
Moraes Barros RR, Straimer J, Sa JM, Salzman RE, Melendez-Muniz VA, Mu J et al (2015) Editing the Plasmodium vivax genome, using zinc-finger nucleases. J Infect Dis 211(1):125–129. https://doi.org/10.1093/infdis/jiu423 . PubMed PMID: 25081932; PubMed Central PMCID: PMCPMC4334824
doi: 10.1093/infdis/jiu423
pubmed: 25081932
Paldi N, Glick E, Oliva M, Zilberberg Y, Aubin L, Pettis J, Chen Y, Evans JD (2010) Effective gene silencing in a microsporidian parasite associated with honeybee (Apis mellifera) colony declines. Appl Environ Microbiol 76(17):5960–5964. PMID: 20622131 PMCID: PMC2935068
doi: 10.1128/AEM.01067-10
Pan G, Xu J, Li T, Xia Q, Liu SL, Zhang G, Li S, Li C, Liu H, Yang L, Liu T, Zhang X, Wu Z, Fan W, Dang X, Xiang H, Tao M, Li Y, Hu J, Li Z, Lin L, Luo J, Geng L, Wang L, Long M, Wan Y, He N, Zhang Z, Lu C, Keeling PJ, Wang J, Xiang Z, Zhou Z (2013) Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC Genomics 14:186. https://doi.org/10.1186/1471-2164-14-186 . PubMed PMID: 23496955; PubMed Central PMCID: PMC3614468
doi: 10.1186/1471-2164-14-186
pubmed: 23496955
pmcid: 3614468
Pan Q, Wang L, Dang X, Ma Z, Zhang X, Chen S, Zhou Z, Xu J (2017) Bacterium-expressed dsRNA downregulates microsporidia Nosema bombycis gene expression. J Eukaryot Microbiol 64(2):278
doi: 10.1111/jeu.12346
Pei B, Wang C, Yu B, Xia D, Li T, Zhou Z (2021) The First Report on the Transovarial Transmission of microsporidian Nosema bombycis in Lepidopteran crop pests Spodoptera litura and Helicoverpa armigera. Microorganisms 9(7):1442. https://doi.org/10.3390/microorganisms9071442 . Epub 2021/08/08. PubMed PMID: 34361877; PubMed Central PMCID: PMCPMC8303212
doi: 10.3390/microorganisms9071442
pubmed: 34361877
pmcid: 8303212
Qian P, Wang X, Yang Z, Li Z, Gao H, Su XZ, Cui H, Yuan J (2018) A Cas9 transgenic Plasmodium yoelii parasite for efficient gene editing. Mol Biochem Parasitol 222:21–28. https://doi.org/10.1016/j.molbiopara.2018.04.003
doi: 10.1016/j.molbiopara.2018.04.003
pubmed: 29684399
Reinke AW, Troemel ER (2015) The development of genetic modification techniques in intracellular parasites and potential applications to microsporidia. PLoS Pathog 11(12):e1005283. https://doi.org/10.1371/journal.ppat.1005283 . PubMed PMID: 26720003; PubMed Central PMCID: PMC4699923
doi: 10.1371/journal.ppat.1005283
pubmed: 26720003
pmcid: 4699923
Rodriguez-Garcia C, Evans JD, Li W, Branchiccela B, Li JH, Heerman MC, Banmeke O, Zhao Y, Hamilton M, Higes M, Martín-Hernández R, Chen YP (2018) Nosemosis control in European honey bees, Apis mellifera, by silencing the gene encoding Nosema ceranae polar tube protein 3. J Exp Biol 221(Pt 19):jeb184606. https://doi.org/10.1242/jeb.184606
doi: 10.1242/jeb.184606
pubmed: 30135088
Shen B, Brown KM, Lee TD, Sibley LD (2014) Efficient gene disruption in diverse strains of Toxoplasma gondii using CRISPR/CAS9. MBio 5(3):e01114–e01114. https://doi.org/10.1128/mBio.01114-14 . PMID: 24825012 PMCID: PMC4030483
doi: 10.1128/mBio.01114-14
pubmed: 24825012
pmcid: 4030483
Sidik SM, Hackett CG, Tran F, Westwood NJ, Lourido S (2014) Efficient genome engineering of Toxoplasma gondii using CRISPR/Cas9. PLoS One 9(6):e100450. https://doi.org/10.1371/journal.pone.0100450 . PubMed PMID: 24971596 PMCID: PMC4074098
doi: 10.1371/journal.pone.0100450
pubmed: 24971596
pmcid: 4074098
Sidik SM, Huet D, Ganesan SM, Huynh MH, Wang T, Nasamu AS, Thiru P, Saeij JPJ, Carruthers VB, Niles JC, Lourido S (2016) A genome-wide CRISPR screen in Toxoplasma identifies essential apicomplexan genes. Cell 166(6):1423–1435. https://doi.org/10.1016/j.cell.2016.08.019 . PMID: 27594426 PMCID: PMC5017925
doi: 10.1016/j.cell.2016.08.019
pubmed: 27594426
pmcid: 5017925
Sin N, Meng L, Wang MQ, Wen JJ, Bornmann WG, Crews CM (1997) The anti-angiogenic agent fumagillin covalently binds and inhibits the methionine aminopeptidase, MetAP-2. Proc Natl Acad Sci U S A 94(12):6099–6103. https://doi.org/10.1073/pnas.94.12.6099 . PubMed PMID: 9177176; PubMed Central PMCID: PMCPMC21008
doi: 10.1073/pnas.94.12.6099
pubmed: 9177176
pmcid: 21008
Soldati D, Boothroyd JC (1993) Transient transfection and expression in the obligate intracellular parasite Toxoplasma gondii. Science 260(5106):349–352
doi: 10.1126/science.8469986
Straimer J, Lee MC, Lee AH, Zeitler B, Williams AE, Pearl JR et al (2012) Site-specific genome editing in Plasmodium falciparum using engineered zinc-finger nucleases. Nat Methods 9(10):993–998. https://doi.org/10.1038/nmeth.2143 . PubMed PMID: 22922501; PubMed Central PMCID: PMCPMC3697006
doi: 10.1038/nmeth.2143
pubmed: 22922501
pmcid: 3697006
Takvorian PM, Buttle KF, Mankus D, Mannella CA, Weiss LM, Cali A (2013) The multilayered interlaced network (MIN) in the sporoplasm of the microsporidium Anncaliia algerae is derived from golgi. J Eukaryot Microbiol 60(2):166–178
doi: 10.1111/jeu.12019
Takvorian PM, Han B, Cali A, Rice WJ, Gunther L, Macaluso F et al (2020) An Ultrastructural study of the extruded polar tube of Anncaliia algerae (Microsporidia). J Eukaryot Microbiol 67(1):28–44. https://doi.org/10.1111/jeu.12751 . Epub 2019/07/25. PubMed PMID: 31332877; PubMed Central PMCID: PMCPMC6944765
doi: 10.1111/jeu.12751
pubmed: 31332877
Vinayak S, Pawlowic MC, Sateriale A, Brooks CF, Studstill CJ, Bar-Peled Y, Cipriano MJ, Striepen B (2015) Genetic modification of the diarrhoeal pathogen Cryptosporidium parvum. Nature 523(7561):477–480. https://doi.org/10.1038/nature14651 . Epub 2015/07/16. PubMed PMID: 26176919; PubMed Central PMCID: PMCPMC4640681
doi: 10.1038/nature14651
pubmed: 26176919
pmcid: 4640681
Wagner JC, Platt RJ, Goldfless SJ, Zhang F, Niles JC (2014) Efficient CRISPR-Cas9-mediated genome editing in Plasmodium falciparum. Nat Methods 11(9):915–918. https://doi.org/10.1038/nmeth.3063 . PubMed PMID: 25108687; PubMed Central PMCID: PMCPMC4199390
doi: 10.1038/nmeth.3063
pubmed: 25108687
pmcid: 4199390
Weidner E, Findley A (1999) Extracellular survival of an intracellular parasite (Spraguea lophii, Microsporea). Biol Bull 197(2):270–271. https://doi.org/10.2307/1542645 . Epub 1999/10/01
doi: 10.2307/1542645
pubmed: 28281795
Weidner E, Trager W (1973) Adenosine triphosphate in the extracellular survival of an intracellular parasite (Nosema michaelis, Microsporidia). J Cell Biol 57(2):586–591. https://doi.org/10.1083/jcb.57.2.586 . Epub 1973/05/01. PubMed PMID: 4633172; PubMed Central PMCID: PMCPMC2108991
doi: 10.1083/jcb.57.2.586
pubmed: 4633172
pmcid: 2108991
Wu YM, Sifri CD, Lei HH, Su XZ, Wellems TE (1995) Transfection of Plasmodium falciparum within human red-blood-cells. P Natl Acad Sci USA 92(4):973–977. https://doi.org/10.1073/pnas.92.4.973 . PMID: 7862676 PMCID: PMC42619
doi: 10.1073/pnas.92.4.973
Wu YM, Kirkman LA, Wellems TE (1996) Transformation of Plasmodium falciparum malaria parasites by homologous integration of plasmids that confer resistance to pyrimethamine. P Natl Acad Sci USA. 93(3):1130–1134. https://doi.org/10.1073/pnas.93.3.1130 . PMID: 8577727 PMCID: PMC40043
doi: 10.1073/pnas.93.3.1130
Young J, Dominicus C, Wagener J, Butterworth S, Ye XD, Kelly G, Ordan M, Saunders B, Instrell R, Howell M, Stewart A, Treeck M (2019) A CRISPR platform for targeted in vivo screens identifies Toxoplasma gondii virulence factors in mice. Nat Commun 10:3963. https://doi.org/10.1038/s41467-019-11855-w . PMID: 31481656 PMCID: PMC6722137
doi: 10.1038/s41467-019-11855-w
pubmed: 31481656
pmcid: 6722137
Zheng SY, Huang YK, Huang HY, Yu B, Zhou N, Wei JH, Pan G, Li C (2021) Zhou Z the role of NbTMP1, a surface protein of sporoplasm, in Nosema bombycis infection. Parasite Vector 14(1):81. https://doi.org/10.1186/s13071-021-04595-8 . PMID: 33494800 PMCID: PMC7836179
doi: 10.1186/s13071-021-04595-8