Establishment and characterization of transformed goat primary cells by expression of simian virus 40 large T antigen for orf virus propagations


Autoři: Yumiko Yamada aff001;  Guan-Ru Liao aff001;  Ching-Yu Tseng aff001;  Yeu-Yang Tseng aff001;  Wei-Li Hsu aff001
Působiště autorů: Graduate Institute of Microbiology and Public Health, National Chung Hsing University, Taichung, Taiwan aff001;  Department of Immunology and Infectious Diseases, John Curtin School of Medical Research, Australian National University, Canberra, Australia aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0226105

Souhrn

Due to the limited host range of orf virus (ORFV), primary cells derived from its natural hosts, such as goats and sheep, are recommended for isolation and propagation of wild type ORFV. This situation limits the option for the study of virus-host interaction during ORFV infection since primary cells only support a few numbers of passages. SV40 T antigen is a viral oncoprotein that can abrogate replicative senescence, leading to an extended life span of cells. In this study, the transformation of two goat primary cells, fibroblast (FB) and testis (GT) cells, were achieved by stably expressing SV40 T antigen using the lentiviral technique. The presence of the gene encoding SV40 T antigen was validated by polymerase chain reaction (PCR) and western blot analyses. As evidenced by immunofluorescent microscopy, the two types of cells expressing SV40 T antigen (namely, FBT and GTT) were purified to homogeneity. Moreover, faster growth kinetics and a lower serum dependency were noticed in FBT and GTT, as compared with their counterpart parental cells. FBT and GTT remain permissive and can form plaque of ORFV, despite with different profiles; generally speaking, with SV40 T expression, ORFV forms plaques with smaller size and distinct margin. Most importantly, the prolonged life span of goat FBT and GTT serves as an ideal cell culture resource for ORFV isolation from the field, studies of ORFV pathogenesis and efficient vaccine development.

Klíčová slova:

Bright field microscopy – Cell immortalization – Fluorescence microscopy – Goats – Polymerase chain reaction – Primary cells – Viral replication – SV40


Zdroje

1. Spyrou V, Valiakos G. Orf virus infection in sheep or goats. Vet Microbiol. 2015;181(1–2):178–82. doi: 10.1016/j.vetmic.2015.08.010 26315771

2. Haig DM. Orf virus infection and host immunity. Curr Opin Infect Dis. 2006;19(2):127–31. doi: 10.1097/01.qco.0000216622.75326.ef 16514336

3. Inoshima Y, Murakami K, Wu D, Sentsui H. Characterization of parapoxviruses circulating among wild Japanese serows (Capricornis crispus). Microbiol Immunol. 2002;46(8):583–7. doi: 10.1111/j.1348-0421.2002.tb02738.x 12363024

4. Billinis C, Mavrogianni VS, Spyrou V, Fthenakis GC. Phylogenetic analysis of strains of Orf virus isolated from two outbreaks of the disease in sheep in Greece. Virol J. 2012;9:24. doi: 10.1186/1743-422X-9-24 22260526

5. Wang R, Wang Y, Liu F, Luo S. Orf virus: A promising new therapeutic agent. Rev Med Virol. 2019;29(1):e2013. doi: 10.1002/rmv.2013 30370570

6. Hosamani M, Scagliarini A, Bhanuprakash V, McInnes CJ, Singh RK. Orf: an update on current research and future perspectives. Expert Rev Anti Infect Ther. 2009;7(7):879–93. doi: 10.1586/eri.09.64 19735227

7. Hosamani M, Yadav S, Kallesh DJ, Mondal B, Bhanuprakash V, Singh RK. Isolation and characterization of an Indian ORF virus from goats. Zoonoses Public Health. 2007;54(5):204–8. doi: 10.1111/j.1863-2378.2007.01046.x 17542963

8. Tryland M, Klein J, Nordoy ES, Blix AS. Isolation and partial characterization of a parapoxvirus isolated from a skin lesion of a Weddell seal. Virus Res. 2005;108(1–2):83–7. doi: 10.1016/j.virusres.2004.08.005 15681058

9. Huda AMASa, Hussein AMAB. Isolation of Orf virus (ORFV) from Iraqi sheep and study the Pathological changes in mice. Int J Curr Microbiol Appl Sci. 2014;3:5.

10. Degraeve C, De Coninck A, Senneseael J, Roseeuw D. Recurrent contagious ecthyma (Orf) in an immunocompromised host successfully treated with cryotherapy. Dermatology. 1999;198(2):162–3. doi: 10.1159/000018095 10325465

11. Lin FY, Tseng YY, Chan KW, Kuo ST, Yang CH, Wang CY, et al. Suppression of influenza virus infection by the orf virus isolated in Taiwan. J Vet Med Sci. 2015;77(9):1055–62. doi: 10.1292/jvms.14-0663 25855509

12. Rintoul JL, Lemay CG, Tai LH, Stanford MM, Falls TJ, de Souza CT, et al. ORFV: a novel oncolytic and immune stimulating parapoxvirus therapeutic. Mol Ther. 2012;20(6):1148–57. doi: 10.1038/mt.2011.301 22273579

13. Cao X, Yang M, Wei RC, Zeng Y, Gu JF, Huang WD, et al. Cancer targeting Gene-Viro-Therapy of liver carcinoma by dual-regulated oncolytic adenovirus armed with TRAIL gene. Gene Ther. 2011;18(8):765–77. doi: 10.1038/gt.2011.16 21412282

14. He B, Huang X, Liu X, Xu B. Cancer targeting gene-viro-therapy for pancreatic cancer using oncolytic adenovirus ZD55-IL-24 in immune-competent mice. Mol Biol Rep. 2013;40(9):5397–405. doi: 10.1007/s11033-013-2638-8 23666064

15. J GP, Levesque S, Workenhe ST, Gujar S, Le Boeuf F, D RC, et al. Trial Watch: Oncolytic viro-immunotherapy of hematologic and solid tumors. Oncoimmunology. 2018;7(12):e1503032. doi: 10.1080/2162402X.2018.1503032 30524901

16. Melzer MK, Lopez-Martinez A, Altomonte J. Oncolytic Vesicular Stomatitis Virus as a Viro-Immunotherapy: Defeating Cancer with a "Hammer" and "Anvil". Biomedicines. 2017;5(1).

17. Workenhe ST, Mossman KL. Rewiring cancer cell death to enhance oncolytic viro-immunotherapy. Oncoimmunology. 2013;2(12):e27138. doi: 10.4161/onci.27138 24498567

18. Xu HN, Huang WD, Cai Y, Ding M, Gu JF, Wei N, et al. HCCS1-armed, quadruple-regulated oncolytic adenovirus specific for liver cancer as a cancer targeting gene-viro-therapy strategy. Mol Cancer. 2011;10:133. doi: 10.1186/1476-4598-10-133 22040050

19. Johnston JB, Barrett JW, Chang W, Chung CS, Zeng W, Masters J, et al. Role of the serine-threonine kinase PAK-1 in myxoma virus replication. J Virol. 2003;77(10):5877–88. doi: 10.1128/JVI.77.10.5877-5888.2003 12719581

20. McFadden G. Poxvirus tropism. Nat Rev Microbiol. 2005;3(3):201–13. doi: 10.1038/nrmicro1099 15738948

21. Fleming SB, Wise LM, Mercer AA. Molecular genetic analysis of orf virus: a poxvirus that has adapted to skin. Viruses. 2015;7(3):1505–39. doi: 10.3390/v7031505 25807056

22. Ivanov L, Hristov M, Peshev R. Studies on cultural characteristics of contagious ecthyma (Orf) virus. Bulgarian Journal of Veterinary Medicine. 2016;19(4):308–16.

23. Mercer AA, Yirrell DL, Reid HW, Robinson AJ. Lack of cross-protection between vaccinia virus and orf virus in hysterectomy-procured, barrier-maintained lambs. Vet Microbiol. 1994;41(4):373–82. doi: 10.1016/0378-1135(94)90033-7 7801537

24. McInnes CJ, Wood AR, Nettleton PE, Gilray JA. Genomic comparison of an avirulent strain of Orf virus with that of a virulent wild type isolate reveals that the Orf virus G2L gene is non-essential for replication. Virus Genes. 2001;22(2):141–50. doi: 10.1023/a:1008117127729 11324750

25. Delhon G, Tulman ER, Afonso CL, Lu Z, de la Concha-Bermejillo A, Lehmkuhl HD, et al. Genomes of the parapoxviruses ORF virus and bovine papular stomatitis virus. J Virol. 2004;78(1):168–77. doi: 10.1128/JVI.78.1.168-177.2004 14671098

26. Klein J, Tryland M. Characterisation of parapoxviruses isolated from Norwegian semi-domesticated reindeer (Rangifer tarandus tarandus). Virol J. 2005;2:79. doi: 10.1186/1743-422X-2-79 16143041

27. Zhang Y, Shi J, Liu S. Establishment and Characterization of a Telomerase-Immortalized Sheep Trophoblast Cell Line. Biomed Res Int. 2016;2016:5808575. doi: 10.1155/2016/5808575 26998488

28. Jin X, Lee JS, Kwak S, Lee SY, Jung JE, Kim TK, et al. Establishment and characterization of three immortal bovine muscular epithelial cell lines. Mol Cells. 2006;21(1):29–33. 16511344

29. Dong F, Huang Y, Li W, Zhao X, Zhang W, Du Q, et al. The isolation and characterization of a telomerase immortalized goat trophoblast cell line. Placenta. 2013;34(12):1243–50. doi: 10.1016/j.placenta.2013.09.009 24112823

30. Munoz-Gutierrez JF, Schneider DA, Baszler TV, Greenlee JJ, Nicholson EM, Stanton JB. hTERT-immortalized ovine microglia propagate natural scrapie isolates. Virus Res. 2015;198:35–43. doi: 10.1016/j.virusres.2014.10.028 25592246

31. Bao L, He L, Chen J, Wu Z, Liao J, Rao L, et al. Reprogramming of ovine adult fibroblasts to pluripotency via drug-inducible expression of defined factors. Cell Res. 2011;21(4):600–8. doi: 10.1038/cr.2011.6 21221129

32. He YL, Wu YH, He XN, Liu FJ, He XY, Zhang Y. An immortalized goat mammary epithelial cell line induced with human telomerase reverse transcriptase (hTERT) gene transfer. Theriogenology. 2009;71(9):1417–24. doi: 10.1016/j.theriogenology.2009.01.012 19303628

33. Bos JL. ras oncogenes in human cancer: a review. Cancer Res. 1989;49(17):4682–9. 2547513

34. Cavender JF, Tevethia MJ. SV40 T-Antigen Amino Acid Changes that Disrupt Cul-7 or Bub-1 Binding Do Not Globally Distort the T-Common Region. Intervirology. 2016;59(1):30–5. doi: 10.1159/000446777 27376672

35. Costa UM, Reischak D, da Silva J, Ravazzolo AP. Establishment and partial characterization of an ovine synovial membrane cell line obtained by transformation with Simian Virus 40 T antigen. J Virol Methods. 2005;128(1–2):72–8. doi: 10.1016/j.jviromet.2005.03.019 15904982

36. Merhi RA, Guillaud L, Delouis C, Cotinot C. Establishment and characterization of immortalized ovine Sertoli cell lines. In Vitro Cell Dev Biol Anim. 2001;37(9):581–8. doi: 10.1290/1071-2690(2001)037<0581:EACOIO>2.0.CO;2 11710435

37. Mselli-Lakhal L, Guiguen F, Fornazero C, Favier C, Durand J, Grezel D, et al. Immortalized goat milk epithelial cell lines replicate CAEV at high level. Vet Res. 2001;32(5):429–40. doi: 10.1051/vetres:2001135 11592613

38. Song Y, Zheng J. Establishment of a Functional Ovine Fetoplacental Artery Endothelial Cell Line with a Prolonged Life Span1. Biol Reprod. 2007;76(1):29–35. doi: 10.1095/biolreprod.106.055921 17005940

39. Zhu H, Ma J, Du R, Zheng L, Wu J, Song W, et al. Characterization of Immortalized Dairy Goat Male Germline Stem Cells (mGSCs). J Cell Biochem. 2014;115(9):1549–60. doi: 10.1002/jcb.24812 24692210

40. Kao C, Wu SQ, DeVries S, Reznikoff WS, Waldman FM, Reznikoff CA. Carcinogen-induced amplification of SV40 DNA inserted at 9q12-21.1 associated with chromosome breakage, deletions, and translocations in human uroepithelial cell transformation in vitro. Genes Chromosomes Cancer. 1993;8(3):155–66. doi: 10.1002/gcc.2870080304 7509623

41. Kao C, Huang J, Wu SQ, Hauser P, Reznikoff CA. Role of SV40 T antigen binding to pRB and p53 in multistep transformation in vitro of human uroepithelial cells. Carcinogenesis. 1993;14(11):2297–302. doi: 10.1093/carcin/14.11.2297 8242858

42. Kao C, Hauser P, Reznikoff WS, Reznikoff CA. Simian virus 40 (SV40) T-antigen mutations in tumorigenic transformation of SV40-immortalized human uroepithelial cells. J Virol. 1993;67(4):1987–95. 8383222

43. Gish WR, Botchan MR. Simian virus 40-transformed human cells that express large T antigens defective for viral DNA replication. J Virol. 1987;61(9):2864–76. 3039174

44. White MKaK, K. Signaling pathways and polyomavirus oncoproteins: Importance in malignant transformation. Gene Ther Mol Bio. 2004;8:19–30.

45. Pipas JM, Levine AJ. Role of T antigen interactions with p53 in tumorigenesis. Semin Cancer Biol. 2001;11(1):23–30. doi: 10.1006/scbi.2000.0343 11243896

46. Ahuja D, Saenz-Robles MT, Pipas JM. SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene. 2005;24(52):7729–45. doi: 10.1038/sj.onc.1209046 16299533

47. Tseng YY, Lin FY, Cheng SF, Tscharke D, Chulakasian S, Chou CC, et al. Functional analysis of the short isoform of orf virus protein OV20.0. J Virol. 2015;89(9):4966–79. doi: 10.1128/JVI.03714-14 25694596

48. Rziha HJ, Buttner M, Muller M, Salomon F, Reguzova A, Laible D, et al. Genomic Characterization of Orf Virus Strain D1701-V (Parapoxvirus) and Development of Novel Sites for Multiple Transgene Expression. Viruses. 2019;11(2).

49. Mazur C, Machado RD. Detection of contagious pustular dermatitis virus of goats in a severe outbreak. Vet Rec. 1989;125(16):419–20. doi: 10.1136/vr.125.16.419 2588444

50. Gelaye E, Achenbach JE, Jenberie S, Ayelet G, Belay A, Yami M, et al. Molecular characterization of orf virus from sheep and goats in Ethiopia, 2008–2013. Virol J. 2016;13:34. doi: 10.1186/s12985-016-0489-3 26923232

51. Guo J, Rasmussen J, Wunschmann A, de La Concha-Bermejillo A. Genetic characterization of orf viruses isolated from various ruminant species of a zoo. Vet Microbiol. 2004;99(2):81–92. doi: 10.1016/j.vetmic.2003.11.010 15019099

52. Oem JK, Chung JY, Kim YJ, Lee KK, Kim SH, Jung BY, et al. Isolation and characterization of orf viruses from Korean black goats. J Vet Sci. 2013;14(2):227–30. doi: 10.4142/jvs.2013.14.2.227 23814477

53. Chan KW, Hsu WL, Wang CY, Yang CH, Lin FY, Chulakasian S, et al. Differential diagnosis of orf viruses by a single-step PCR. J Virol Methods. 2009;160(1–2):85–9. doi: 10.1016/j.jviromet.2009.04.025 19409929

54. Lin FY, Chan KW, Wang CY, Wong ML, Hsu WL. Purification and functional motifs of the recombinant ATPase of orf virus. Protein Expr Purif. 2011;79(2):210–6. doi: 10.1016/j.pep.2011.04.010 21540113

55. Kenner J, Cameron F, Empig C, Jobes DV, Gurwith M. LC16m8: an attenuated smallpox vaccine. Vaccine. 2006;24(47–48):7009–22. doi: 10.1016/j.vaccine.2006.03.087 17052815

56. Sanchez-Sampedro L, Gomez CE, Mejias-Perez E, Perez-Jimenez E, Oliveros JC, Esteban M. Attenuated and replication-competent vaccinia virus strains M65 and M101 with distinct biology and immunogenicity as potential vaccine candidates against pathogens. J Virol. 2013;87(12):6955–74. doi: 10.1128/JVI.03013-12 23596295

57. McCurdy LH, Larkin BD, Martin JE, Graham BS. Modified vaccinia Ankara: potential as an alternative smallpox vaccine. Clin Infect Dis. 2004;38(12):1749–53. doi: 10.1086/421266 15227622

58. Mayr A, Herlyn M, Mahnel H, Danco A, Zach A, Bostedt H. [Control of ecthyma contagiosum (pustular dermatitis) of sheep with a new parenteral cell culture live vaccine]. Zentralbl Veterinarmed B. 1981;28(7):535–52. 7331595

59. Cottone R, Buttner M, Bauer B, Henkel M, Hettich E, Rziha HJ. Analysis of genomic rearrangement and subsequent gene deletion of the attenuated Orf virus strain D1701. Virus Res. 1998;56(1):53–67. doi: 10.1016/s0168-1702(98)00056-2 9784065

60. Rziha HJ, Rohde J, Amann R. Generation and Selection of Orf Virus (ORFV) Recombinants. Methods Mol Biol. 2016;1349:177–200. doi: 10.1007/978-1-4939-3008-1_12 26458837

61. Hubbard K, Ozer HL. Mechanism of immortalization. Age (Omaha). 1999;22(2):65–9.

62. Shay JW, Wright WE. Quantitation of the frequency of immortalization of normal human diploid fibroblasts by SV40 large T-antigen. Exp Cell Res. 1989;184(1):109–18. doi: 10.1016/0014-4827(89)90369-8 2551703

63. Duncan MR, Stanish SM, Cox DC. Differential sensitivity of normal and transformed human cells to reovirus infection. J Virol. 1978;28(2):444–9. 214572

64. Zhong P, Agosto LM, Munro JB, Mothes W. Cell-to-cell transmission of viruses. Curr Opin Virol. 2013;3(1):44–50. doi: 10.1016/j.coviro.2012.11.004 23219376

65. Chen P, Hubner W, Spinelli MA, Chen BK. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J Virol. 2007;81(22):12582–95. doi: 10.1128/JVI.00381-07 17728240

66. Platt EJ, Kozak SL, Durnin JP, Hope TJ, Kabat D. Rapid dissociation of HIV-1 from cultured cells severely limits infectivity assays, causes the inactivation ascribed to entry inhibitors, and masks the inherently high level of infectivity of virions. J Virol. 2010;84(6):3106–10. doi: 10.1128/JVI.01958-09 20042508


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