Article: | MedLuna.com

Overview

Journal Genes (Basel)

Publisher MDPI

Date 2019 Mar 23

PMID 30897824

Citations 8

Authors

Efstathios S Giotis

Guillaume Montillet

Bertrand Pain

Michael A Skinner

Affiliations

Soon will be listed here.

Abstract

The discovery of mammalian pluripotent embryonic stem cells (ESC) has revolutionised cell research and regenerative medicine. More recently discovered chicken ESC (cESC), though less intensively studied, are increasingly popular as vaccine substrates due to a dearth of avian cell lines. Information on the comparative performance of cESC with common vaccine viruses is limited. Using RNA-sequencing, we compared cESC transcriptional programmes elicited by stimulation with chicken type I interferon or infection with vaccine viruses routinely propagated in primary chicken embryo fibroblasts (CEF). We used poxviruses (fowlpox virus (FWPV) FP9, canarypox virus (CNPV), and modified vaccinia virus Ankara (MVA)) and a birnavirus (infectious bursal disease virus (IBDV) PBG98). Interferon-stimulated genes (ISGs) were induced in cESC to levels comparable to those in CEF and immortalised chicken fibroblast DF-1 cells. cESC are permissive (with distinct host transcriptional responses) to MVA, FP9, and CNPV but, surprisingly, not to PBG98. MVA CNPV, and FP9 suppressed innate immune responses, while PBG98 induced a subset of ISGs. Dysregulation of signalling pathways (i.e., NFκB, TRAF) was observed, which might affect immune responses and viral replication. In conclusion, we show that cESC are an attractive alternative substrate to study and propagate poxvirus recombinant vaccine vectors.

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References

Brown S, Mehtali M . The Avian EB66(R) Cell Line, Application to Vaccines, and Therapeutic Protein Production. PDA J Pharm Sci Technol. 2011; 64(5):419-25. View

Dulwich K, Giotis E, Gray A, Nair V, Skinner M, Broadbent A . Differential gene expression in chicken primary B cells infected ex vivo with attenuated and very virulent strains of infectious bursal disease virus (IBDV). J Gen Virol. 2017; 98(12):2918-2930. DOI: 10.1099/jgv.0.000979. View

Buttigieg K, Laidlaw S, Ross C, Davies M, Goodbourn S, Skinner M . Genetic screen of a library of chimeric poxviruses identifies an ankyrin repeat protein involved in resistance to the avian type I interferon response. J Virol. 2013; 87(9):5028-40. PMC: 3624283. DOI: 10.1128/JVI.02738-12. View

Giotis E, Skinner M . Spotlight on avian pathology: fowlpox virus. Avian Pathol. 2018; 48(2):87-90. DOI: 10.1080/03079457.2018.1554893. View

STICKL H, Hochstein-Mintzel V, Mayr A, Huber H, Schafer H, Holzner A . [MVA vaccination against smallpox: clinical tests with an attenuated live vaccinia virus strain (MVA) (author's transl)]. Dtsch Med Wochenschr. 1974; 99(47):2386-92. DOI: 10.1055/s-0028-1108143. View

Fuet A, Pain B . Chicken Induced Pluripotent Stem Cells: Establishment and Characterization. Methods Mol Biol. 2017; 1650:211-228. DOI: 10.1007/978-1-4939-7216-6_14. View

Naruse T, Fukuda T, Tanabe T, Ichikawa M, Oda Y, Tochihara S . A clinical phase I study of an EB66 cell-derived H5N1 pandemic vaccine adjuvanted with AS03. Vaccine. 2015; 33(45):6078-84. DOI: 10.1016/j.vaccine.2015.09.022. View

Fernandez-Arias A, Risco C, Martinez S, Albar J, Rodriguez J . Expression of ORF A1 of infectious bursal disease virus results in the formation of virus-like particles. J Gen Virol. 1998; 79 ( Pt 5):1047-54. DOI: 10.1099/0022-1317-79-5-1047. View

Jordan I, Vos A, Beilfuss S, Neubert A, Breul S, Sandig V . An avian cell line designed for production of highly attenuated viruses. Vaccine. 2008; 27(5):748-56. DOI: 10.1016/j.vaccine.2008.11.066. View

10.

Brown M, Skinner M . Coding sequences of both genome segments of a European 'very virulent' infectious bursal disease virus. Virus Res. 1996; 40(1):1-15. DOI: 10.1016/0168-1702(95)01253-2. View

11.

Ivashkiv L, Donlin L . Regulation of type I interferon responses. Nat Rev Immunol. 2013; 14(1):36-49. PMC: 4084561. DOI: 10.1038/nri3581. View

12.

Olivier S, Jacoby M, Brillon C, Bouletreau S, Mollet T, Nerriere O . EB66 cell line, a duck embryonic stem cell-derived substrate for the industrial production of therapeutic monoclonal antibodies with enhanced ADCC activity. MAbs. 2010; 2(4):405-15. PMC: 3180087. DOI: 10.4161/mabs.12350. View

13.

Liem J, Liu J . Stress Beyond Translation: Poxviruses and More. Viruses. 2016; 8(6). PMC: 4926189. DOI: 10.3390/v8060169. View

14.

Pain B, Clark M, Shen M, Nakazawa H, Sakurai M, Samarut J . Long-term in vitro culture and characterisation of avian embryonic stem cells with multiple morphogenetic potentialities. Development. 1996; 122(8):2339-48. DOI: 10.1242/dev.122.8.2339. View

15.

Laidlaw S, Robey R, Davies M, Giotis E, Ross C, Buttigieg K . Genetic screen of a mutant poxvirus library identifies an ankyrin repeat protein involved in blocking induction of avian type I interferon. J Virol. 2013; 87(9):5041-52. PMC: 3624286. DOI: 10.1128/JVI.02736-12. View

16.

Vandepoele K, Saeys Y, Simillion C, Raes J, Van de Peer Y . The automatic detection of homologous regions (ADHoRe) and its application to microcolinearity between Arabidopsis and rice. Genome Res. 2002; 12(11):1792-801. PMC: 187543. DOI: 10.1101/gr.400202. View

17.

Giotis E, Scott A, Rothwell L, Hu T, Talbot R, Todd D . Chicken anaemia virus evades host immune responses in transformed lymphocytes. J Gen Virol. 2018; 99(3):321-327. DOI: 10.1099/jgv.0.001011. View

18.

Xie P . TRAF molecules in cell signaling and in human diseases. J Mol Signal. 2013; 8(1):7. PMC: 3697994. DOI: 10.1186/1750-2187-8-7. View

19.

Qu H, Yang L, Meng S, Xu L, Bi Y, Jia X . The differential antiviral activities of chicken interferon α (ChIFN-α) and ChIFN-β are related to distinct interferon-stimulated gene expression. PLoS One. 2013; 8(3):e59307. PMC: 3602166. DOI: 10.1371/journal.pone.0059307. View

20.

Jean C, Oliveira N, Intarapat S, Fuet A, Mazoyer C, De Almeida I . Transcriptome analysis of chicken ES, blastodermal and germ cells reveals that chick ES cells are equivalent to mouse ES cells rather than EpiSC. Stem Cell Res. 2014; 14(1):54-67. PMC: 4305369. DOI: 10.1016/j.scr.2014.11.005. View