Login Register Cart 0
Research Article

Evaluation of the Nucleopolyhedrovirus of Anticarsia gemmatalis as a Vector for Gene Therapy in Mammals

Author(s): Cintia N. Parsza, Diego L.M. Gómez, Jorge A. Simonin, Mariano Nicolás Belaich* and Pablo D. Ghiringhelli

Volume 21, Issue 2, 2021

Published on: 17 December, 2020

Page: [177 - 189] Pages: 13

DOI: 10.2174/1566523220999201217155945

Price: $65

Open Access Journals Promotions 2
Abstract

Background: Baculoviruses are insect pathogens with important biotechnological applications that transcend their use as biological controllers of agricultural pests. One species, Autographa californica multiple nucleopolhyedrovirus (AcMNPV), has been extensively exploited as a molecular platform to produce recombinant proteins and as a delivery vector for genes in mammals because it can transduce a wide range of mammalian cells and tissues without replicating or producing progeny.

Method: To investigate if the budded virions of Anticarsia gemmatalis multiple nucleopolhyedrovirus (AgMNPV) species has the same ability, the viral genome was modified by homologous recombination into susceptible insect cells to integrate reporter genes and then it was evaluated on mammalian cell lines in a comparative form with respect to equivalent viruses derived from AcMNPV. Besides, the replicative capacity of AgMNPV´s virions in mammals was determined.

Results: The experiments carried out showed that the recombinant variant of AgMNPV transduces and support the expression of delivered genes but not replicates in mammalian cells.

Conclusion: Consequently, this insect pathogen is proposed as an alternative to non-infectious viruses in humans to explore new approaches in gene therapy and other applications based on the use of mammalian cells.

Keywords: Baculovirus, AgMNPV, AcMNPV, BacMam, transduction, gene therapy.

« Previous
Graphical Abstract

[1]
Nayerossadat N, Maedeh T, Ali PA. Viral and nonviral delivery systems for gene delivery. Adv Biomed Res 2012; 1: 27.
[http://dx.doi.org/10.4103/2277-9175.98152] [PMID: 23210086]
[2]
Anguela XM, High KA. Entering the modern era of gene therapy. Annu Rev Med 2019; 70: 273-88.
[http://dx.doi.org/10.1146/annurev-med-012017-043332] [PMID: 30477394]
[3]
Lundstrom K, Boulikas T. Viral and non-viral vectors in gene therapy: technology development and clinical trials. Technol Cancer Res Treat 2003; 2(5): 471-86.
[http://dx.doi.org/10.1177/153303460300200513] [PMID: 14529313]
[4]
Jiao Y, Xia ZL, Ze LJ, Jing H, Xin B, Fu S. Research Progress of nucleic acid delivery vectors for gene therapy. Biomed Microdevices 2020; 22(1): 16.
[http://dx.doi.org/10.1007/s10544-020-0469-7] [PMID: 31989315]
[5]
Naldini L. Ex vivo gene transfer and correction for cell-based therapies. Nat Rev Genet 2011; 12(5): 301-15.
[http://dx.doi.org/10.1038/nrg2985] [PMID: 21445084]
[6]
Gowing G, Svendsen S, Svendsen CN. Ex vivo gene therapy for the treatment of neurological disorders. In: Prog Brain Res. 2017; 230: pp. 99-132.
[http://dx.doi.org/10.1016/bs.pbr.2016.11.003] [PMID: 28552237]
[7]
Martínez-Morales PL, Revilla A, Ocaña I, et al. Progress in stem cell therapy for major human neurological disorders. Stem Cell Rev Rep 2013; 9(5): 685-99.
[http://dx.doi.org/10.1007/s12015-013-9443-6] [PMID: 23681704]
[8]
Tani K. Current status of ex vivo gene therapy for hematological disorders: a review of clinical trials in Japan around the world. Int J Hematol 2016; 104(1): 42-72.
[http://dx.doi.org/10.1007/s12185-016-2030-2] [PMID: 27289360]
[9]
Yang G, Lv F, Wang B, Liu L, Yang Q, Wang S. Multifunctional non-viral delivery systems based on conjugated polymers. Macromol Biosci 2012; 12(12): 1600-14.
[http://dx.doi.org/10.1002/mabi.201200267] [PMID: 23161784]
[10]
Jones CH, Chen CK, Ravikrishnan A, Rane S, Pfeifer BA. Overcoming nonviral gene delivery barriers: perspective and future. Mol Pharm 2013; 10(11): 4082-98.
[http://dx.doi.org/10.1021/mp400467x] [PMID: 24093932]
[11]
Dorraj G, Carreras JJ, Nunez H, Abushammala I, Melero A. Lipid Nanoparticles as Potential Gene Therapeutic Delivery Systems for Oral Administration. Curr Gene Ther 2017; 17(2): 89-104.
[http://dx.doi.org/10.2174/1566523217666170510163038] [PMID: 28494737]
[12]
Waehler R, Russell SJ, Curiel DT. Engineering targeted viral vectors for gene therapy. Nat Rev Genet 2007; 8(8): 573-87.
[http://dx.doi.org/10.1038/nrg2141] [PMID: 17607305]
[13]
Asad AS, Moreno Ayala MA, Gottardo MF, et al. Viral gene therapy for breast cancer: progress and challenges. Expert Opin Biol Ther 2017; 17(8): 945-59.
[http://dx.doi.org/10.1080/14712598.2017.1338684] [PMID: 28604109]
[14]
Lundstrom K. Viral vectors in gene therapy. Diseases 2018; 6(2): 42.
[http://dx.doi.org/10.3390/diseases6020042] [PMID: 29883422]
[15]
Ehrke-Schulz E, Zhang W, Schiwon M, et al. Cloning and largescale production of high-capacity adenoviral vectors based on the human adenovirus type 5. J Vis Exp 2016; 28(107)e52894
[PMID: 26863087]
[16]
Yamamoto Y, Nagasato M, Yoshida T, Aoki K. Recent advances in genetic modification of adenovirus vectors for cancer treatment. Cancer Sci 2017; 108(5): 831-7.
[http://dx.doi.org/10.1111/cas.13228] [PMID: 28266780]
[17]
Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 2011; 12(5): 341-55.
[http://dx.doi.org/10.1038/nrg2988] [PMID: 21499295]
[18]
Samulski RJ, Muzyczka N. AAV-mediated gene therapy for research and therapeutic purposes. Annu Rev Virol 2014; 1(1): 427-51.
[http://dx.doi.org/10.1146/annurev-virology-031413-085355] [PMID: 26958729]
[19]
Choudhury SR, Fitzpatrick Z, Harris AF, et al. In Vivo selection yields AAV-B1 capsid for central nervous system and muscle gene therapy. Mol Ther 2016; 24(7): 1247-57.
[http://dx.doi.org/10.1038/mt.2016.84] [PMID: 27117222]
[20]
Coroadinha AS, Gama-Norton L, Amaral AI, Hauser H, Alves PM, Cruz PE. Production of retroviral vectors. [review Curr Gene Ther 2010; 10(6): 456-73.
[http://dx.doi.org/10.2174/156652310793797739] [PMID: 21054246]
[21]
Schambach A, Morgan M. Retroviral vectors for cancer gene therapy. Recent Results Cancer Res 2016; 209: 17-35.
[http://dx.doi.org/10.1007/978-3-319-42934-2_2] [PMID: 28101685]
[22]
Thomas CE, Ehrhardt A, Kay MA. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 2003; 4(5): 346-58.
[http://dx.doi.org/10.1038/nrg1066] [PMID: 12728277]
[23]
Zaiss AK, Machado HB, Herschman HR. The influence of innate and pre-existing immunity on adenovirus therapy. J Cell Biochem 2009; 108(4): 778-90.
[http://dx.doi.org/10.1002/jcb.22328] [PMID: 19711370]
[24]
Hendrickx R, Stichling N, Koelen J, Kuryk L, Lipiec A, Greber UF. Innate immunity to adenovirus. Hum Gene Ther 2014; 25(4): 265-84.
[http://dx.doi.org/10.1089/hum.2014.001] [PMID: 24512150]
[25]
Airenne KJ, Makkonen KE, Mähönen AJ, Ylä-Herttuala S. Baculoviruses mediate efficient gene expression in a wide range of vertebrate cells. Methods Mol Biol 2011; 737: 279-301.
[http://dx.doi.org/10.1007/978-1-61779-095-9_12] [PMID: 21590402]
[26]
Ono C, Okamoto T, Abe T, Matsuura Y. Baculovirus as a tool for gene delivery and gene therapy. Viruses 2018; 10(9): 510.
[http://dx.doi.org/10.3390/v10090510] [PMID: 30235841]
[27]
Rohrmann GF. Baculovirus Molecular Biology. 4th ed. National Center for Biotechnology Information Bethesda 2019.
[28]
Szewczyk B, Rabalski L, Krol E, Sihler W. Lobo de Souza M. Baculovirus biopesticides - A safe alternative to chemical protection of plants. J Biopesticides 2009; 2(2): 209-16.
[29]
Haase S, Sciocco-Cap A, Romanowski V. Baculovirus insecticides in Latin America: historical overview, current status and future perspectives. Viruses 2015; 7(5): 2230-67.
[http://dx.doi.org/10.3390/v7052230] [PMID: 25941826]
[30]
Condreay JP, Kost TA. Baculovirus expression vectors for insect and mammalian cells. Curr Drug Targets 2007; 8(10): 1126-31.
[http://dx.doi.org/10.2174/138945007782151351] [PMID: 17979672]
[31]
van Oers MM, Pijlman GP, Vlak JM. Thirty years of baculovirus-insect cell protein expression: from dark horse to mainstream technology. J Gen Virol 2015; 96(Pt 1): 6-23.
[http://dx.doi.org/10.1099/vir.0.067108-0] [PMID: 25246703]
[32]
Airenne KJ, Hu YC, Kost TA, et al. Baculovirus: an insect-derived vector for diverse gene transfer applications. Mol Ther 2013; 21(4): 739-49.
[http://dx.doi.org/10.1038/mt.2012.286] [PMID: 23439502]
[33]
Mansouri M, Berger P. Baculovirus for gene delivery to mammalian cells: Past, present and future. Plasmid 2018; 98: 1-7.
[http://dx.doi.org/10.1016/j.plasmid.2018.05.002] [PMID: 29842913]
[34]
Thimiri Govinda Raj DB, Khan NA, Venkatachalam S, Arumugam S. BacMam System for rapid recombinant protein expression in mammalian cells. Methods Mol Biol 2020; 2125: 205-8.
[http://dx.doi.org/10.1007/7651_2019_249] [PMID: 31228126]
[35]
Sung LY, Chen CL, Lin SY, et al. Efficient gene delivery into cell lines and stem cells using baculovirus. Nat Protoc 2014; 9(8): 1882-99.
[http://dx.doi.org/10.1038/nprot.2014.130] [PMID: 25010908]
[36]
Tjia ST, zu Altenschildesche GM, Doerfler W. Autographa californica nuclear polyhedrosis virus (AcNPV) DNA does not persist in mass cultures of mammalian cells. Virology 1983; 125(1): 107-17.
[http://dx.doi.org/10.1016/0042-6822(83)90067-3] [PMID: 6402854]
[37]
Kost TA, Condreay JP. Innovations-Biotechnology: Baculovirus vectors as gene transfer vectors for mammalian cells: Biosafety considerations. J Am Biol Saf Assoc 2002; 7(3): 167-9.
[http://dx.doi.org/10.1177/153567600200700312]
[38]
Gronowski AM, Hilbert DM, Sheehan KC, Garotta G, Schreiber RD. Baculovirus stimulates antiviral effects in mammalian cells. J Virol 1999; 73(12): 9944-51.
[http://dx.doi.org/10.1128/JVI.73.12.9944-9951.1999] [PMID: 10559307]
[39]
Abe T, Takahashi H, Hamazaki H, Miyano-Kurosaki N, Matsuura Y, Takaku H. Baculovirus induces an innate immune response and confers protection from lethal influenza virus infection in mice. J Immunol 2003; 171(3): 1133-9.
[http://dx.doi.org/10.4049/jimmunol.171.3.1133] [PMID: 12874198]
[40]
Abe T, Hemmi H, Miyamoto H, et al. Involvement of the Toll-like receptor 9 signaling pathway in the induction of innate immunity by baculovirus. J Virol 2005; 79(5): 2847-58.
[http://dx.doi.org/10.1128/JVI.79.5.2847-2858.2005] [PMID: 15709004]
[41]
Abe T, Kaname Y, Wen X, et al. Baculovirus induces type I interferon production through toll-like receptor-dependent and -independent pathways in a cell-type-specific manner. J Virol 2009; 83(15): 7629-40.
[http://dx.doi.org/10.1128/JVI.00679-09] [PMID: 19474102]
[42]
Bocca AL, Barros MC, Martins GK, et al. Immunological effects of Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV) by stimulation of mice in vivo and in vitro. Virus Res 2013; 176(1-2): 119-27.
[http://dx.doi.org/10.1016/j.virusres.2013.05.015] [PMID: 23747526]
[43]
Cheshenko N, Krougliak N, Eisensmith RC, Krougliak VA. A novel system for the production of fully deleted adenovirus vectors that does not require helper adenovirus. Gene Ther 2001; 8(11): 846-54.
[http://dx.doi.org/10.1038/sj.gt.3301459] [PMID: 11423932]
[44]
Luckow VA, Lee SC, Barry GF, Olins PO. Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J Virol 1993; 67(8): 4566-79.
[http://dx.doi.org/10.1128/JVI.67.8.4566-4579.1993] [PMID: 8392598]
[45]
Yao Lg, Sun Jc, Xu H. Kan Yc, Zhang Xm, Yan HC. A novel economic method for high throughput production of recombinant baculovirus by infecting insect cells with Bacmid-containing diminopimelate-auxotrophic Escherichia coli. J Biotechnol 2010; 145(1): 23-9.
[http://dx.doi.org/10.1016/j.jbiotec.2009.10.003] [PMID: 19835917]
[46]
Buchholz CJ, Friedel T, Büning H. Surface-engineered viral vectors for selective and cell type-specific gene delivery. Trends Biotechnol 2015; 33(12): 777-90.
[http://dx.doi.org/10.1016/j.tibtech.2015.09.008] [PMID: 26497425]
[47]
Kenoutis C, Efrose RC, Swevers L, et al. Baculovirus-mediated gene delivery into Mammalian cells does not alter their transcriptional and differentiating potential but is accompanied by early viral gene expression. J Virol 2006; 80(8): 4135-46.
[http://dx.doi.org/10.1128/JVI.80.8.4135-4146.2006] [PMID: 16571829]
[48]
Liu X, Li Y, Hu X, Yi Y, Zhang Z. Gene delivery and gene expression in vertebrate using baculovirus Bombyx mori nucleopolyhedrovirus vector. Oncotarget 2017; 8(62): 106017-25.
[http://dx.doi.org/10.18632/oncotarget.22522] [PMID: 29285311]
[49]
Kataoka C, Kaname Y, Taguwa S, et al. Baculovirus GP64-mediated entry into mammalian cells. J Virol 2012; 86(5): 2610-20.
[http://dx.doi.org/10.1128/JVI.06704-11] [PMID: 22190715]
[50]
Westenberg M, Uijtdewilligen P, Vlak JM. Baculovirus envelope fusion proteins F and GP64 exploit distinct receptors to gain entry into cultured insect cells. J Gen Virol 2007; 88(Pt 12): 3302-6.
[http://dx.doi.org/10.1099/vir.0.83240-0] [PMID: 18024899]
[51]
Luz-Madrigal A, Asanov A, Camacho-Zarco AR, Sampieri A, Vaca L. A cholesterol recognition amino acid consensus domain in GP64 fusion protein facilitates anchoring of baculovirus to mammalian cells. J Virol 2013; 87(21): 11894-907.
[http://dx.doi.org/10.1128/JVI.01356-13] [PMID: 23986592]
[52]
Harrison RL, Herniou EA, Jehle JA, et al. Ictv Report Consortium. ICTV Virus Taxonomy Profile: Baculoviridae. J Gen Virol 2018; 99(9): 1185-6.
[http://dx.doi.org/10.1099/jgv.0.001107] [PMID: 29947603]
[53]
Jehle JA, Lange M, Wang H, Hu Z, Wang Y, Hauschild R. Molecular identification and phylogenetic analysis of baculoviruses from Lepidoptera. Virology 2006; 346(1): 180-93.
[http://dx.doi.org/10.1016/j.virol.2005.10.032] [PMID: 16313938]
[54]
Miele SA, Garavaglia MJ, Belaich MN, Ghiringhelli PD. Baculovirus: molecular insights on their diversity and conservation. Int J Evol Biol 2011; 2011379424
[http://dx.doi.org/10.4061/2011/379424] [PMID: 21716740]
[55]
Allen G, Knell JD. A nuclear polyhedrosis virus of Anticarsia gemmatalis: Ultrastructure, replication and pathogenicity. Fla Entomol 1977; 60(3): 233-40.
[http://dx.doi.org/10.2307/3493914]
[56]
Moscardi F. A Nucleopolyhedrovirus for control of the velvetbean caterpillar in Brazilian SoybeansBiological Control: A Global Perspective. Wallingford, UK: CAB International 2007; pp. 344-52.
[http://dx.doi.org/10.1079/9781845932657.0344]
[57]
Oliveira JVC, Wolff JLC, Garcia-Maruniak A, et al. Genome of the most widely used viral biopesticide: Anticarsia gemmatalis multiple nucleopolyhedrovirus. J Gen Virol 2006; 87(Pt 11): 3233-50.
[http://dx.doi.org/10.1099/vir.0.82161-0] [PMID: 17030857]
[58]
Sieburth PJ, Maruniak JE. Growth characteristic of a continuous cell line from the velvetbean caterpillar Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae). In Vitro Cell Dev Biol 1988; 24: 195-8.
[http://dx.doi.org/10.1007/BF02623546]
[59]
Sieburth PJ, Maruniak JE. Susceptibility of an established cell line of Anticarsia gemmatalis (Lepidoptera: Noctuidae) to three nuclear polyhedrosis viruses. J Invertebr Pathol 1988; 52(3): 453-8.
[http://dx.doi.org/10.1016/0022-2011(88)90058-4]
[60]
Vaughn JL, Goodwin RH, Tompkins GJ, McCawley P. The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). In Vitro 1977; 13(4): 213-7.
[http://dx.doi.org/10.1007/BF02615077] [PMID: 68913]
[61]
King L, Possee R. Propagation, titration and purification of AcMNPV in cell cultureThe Baculovirus Expression System: A Laboratory Guide. London: Chapman & Hall 1992; pp. 106-26.
[http://dx.doi.org/10.1007/978-94-011-2374-7_6]
[62]
O’Reilly DR, Miller L, Luckow VA. Baculovirus Expression Vectors: A Laboratory Manual. New York: Oxford University Press 1994.
[63]
Kwang TW, Zeng X, Wang S. Manufacturing of AcMNPV baculovirus vectors to enable gene therapy trials. Mol Ther Methods Clin Dev 2016; 3: 15050.
[http://dx.doi.org/10.1038/mtm.2015.50] [PMID: 26858963]
[64]
Green MR, Sambrook J. Molecular Cloning: A laboratory manual. 4th ed. New York: Cold Spring Harbor Laboratory Press 2012.
[65]
Domier LL, McCoppin NK, D’Arcy CJ. Sequence requirements for translation initiation of Rhopalosiphum padi virus ORF2. Virology 2000; 268(2): 264-71.
[http://dx.doi.org/10.1006/viro.2000.0189] [PMID: 10704335]
[66]
Wu YJ, Teng CY, Chen YJ, et al. Internal ribosome entry site of Rhopalosiphum padi virus is functional in mammalian cells and has cryptic promoter activity in baculovirus-infected Sf21 cells. Acta Pharmacol Sin 2008; 29(8): 965-74.
[http://dx.doi.org/10.1111/j.1745-7254.2008.00820.x] [PMID: 18664329]
[67]
Nasimuzzaman M, van der Loo JCM, Malik P. Production and Purification of Baculovirus for Gene Therapy Application. J Vis Exp 2018; 134(134): 57019.
[http://dx.doi.org/10.3791/57019] [PMID: 29683451]
[68]
Larkin MA, Blackshields G, Brown NP, et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23(21): 2947-8.
[http://dx.doi.org/10.1093/bioinformatics/btm404] [PMID: 17846036]
[69]
Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 2016; 33(7): 1870-4.
[http://dx.doi.org/10.1093/molbev/msw054] [PMID: 27004904]
[70]
Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14(6): 1188-90.
[http://dx.doi.org/10.1101/gr.849004] [PMID: 15173120]
[71]
Telford WG, Hawley T, Subach F, Verkhusha V, Hawley RG. Flow cytometry of fluorescent proteins. Methods 2012; 57(3): 318-30.
[http://dx.doi.org/10.1016/j.ymeth.2012.01.003] [PMID: 22293036]
[72]
FlowJo™ Software for Windows Version 762 2019.
[73]
Singh C, Roy-Chowdhuri S. Quantitative Real-Time PCR: Recent Advances. Methods Mol Biol 2016; 1392: 161-76.
[http://dx.doi.org/10.1007/978-1-4939-3360-0_15] [PMID: 26843055]
[74]
Miele SAB, Cerrudo CS, Parsza CN, et al. Identification of Multiple Replication Stages and Origins in the Nucleopolyhedrovirus of Anticarsia gemmatalis. Viruses 2019; 11(7): 648.
[http://dx.doi.org/10.3390/v11070648] [PMID: 31311127]
[75]
Jorio H, Tran R, Meghrous J, Bourget L, Kamen A. Analysis of baculovirus aggregates using flow cytometry. J Virol Methods 2006; 134(1-2): 8-14.
[http://dx.doi.org/10.1016/j.jviromet.2005.11.009] [PMID: 16364459]
[76]
Yu IL, Lin YC, Robinson JH, Lung O. Transduction of vertebrate cells with Spodoptera exigua multiple nucleopolyhedrovirus F protein-pseudotyped gp64-null Autographa californica multiple nucleopolyhedrovirus. J Gen Virol 2009; 90(Pt 9): 2282-7.
[http://dx.doi.org/10.1099/vir.0.012138-0] [PMID: 19474242]
[77]
Blissard GW, Theilmann DA. Baculovirus Entry and Egress from Insect Cells. Annu Rev Virol 2018; 5(1): 113-39.
[http://dx.doi.org/10.1146/annurev-virology-092917-043356] [PMID: 30004832]
[78]
Holliday DL, Speirs V. Choosing the right cell line for breast cancer research. Breast Cancer Res 2011; 13(4): 215.
[http://dx.doi.org/10.1186/bcr2889] [PMID: 21884641]
[79]
Mengual Gómez DL, Belaich MN, Rodríguez VA, Ghiringhelli PD. Effects of fetal bovine serum deprivation in cell cultures on the production of Anticarsia gemmatalis multinucleopolyhedrovirus. BMC Biotechnol 2010; 10: 68.
[http://dx.doi.org/10.1186/1472-6750-10-68] [PMID: 20843354]
[80]
Micheloud GA, Gioria VV, Eberhardt I, Visnovsky G, Claus JD. Production of the Anticarsia gemmatalis multiple nucleopolyhedrovirus in serum-free suspension cultures of the saUFL-AG-286 cell line in stirred reactor and airlift reactor. J Virol Methods 2011; 178(1-2): 106-16.
[http://dx.doi.org/10.1016/j.jviromet.2011.08.024] [PMID: 21906626]

Rights & Permissions Print Cite
Article Metrics
28
1
Wayfinder Image
Open Access Journals Promotions
© 2024 Bentham Science Publishers | Privacy Policy