Top

Published in:

01-04-2018 | Brief Report

Polymerase chain reaction-based detection of myc transduction in feline leukemia virus-infected cats

Authors: Ryosuke Sumi, Ariko Miyake, Taiji Endo, Yoshiharu Ohsato, Minh Ha Ngo, Kazuo Nishigaki

Published in: Archives of Virology | Issue 4/2018

Abstract

Feline lymphomas are associated with the transduction and activation of cellular proto-oncogenes, such as c-myc, by feline leukemia virus (FeLV). We describe a polymerase chain reaction assay for detection of myc transduction usable in clinical diagnosis. The assay targets c-myc exons 2 and 3, which together result in a FeLV-specific fusion gene following c-myc transduction. When this assay was conducted on FeLV-infected feline tissues submitted for clinical diagnosis of tumors, myc transduction was detected in 14% of T-cell lymphoma/leukemias. This newly established system could become a useful diagnostic tool in veterinary medicine.

Jarrett WF, Crawford EM, Martin WB, Davie F (1964) A virus-like particle associated with Leukemia (Lymphosarcoma). Nature 202:567–569CrossRef

HardyJr WD (1993) Feline oncoretroviruses. In: Levy JA (ed) The retroviridae. Springer Science, New York, pp 109–180CrossRef

Watanabe S, Kawamura M, Odahara Y, Anai Y, Ochi H, Nakagawa S, Endo Y, Tsujimoto H, Nishigaki K (2013) Phylogenetic and structural diversity in the Feline leukemia virus env gene. PLoS One 8:e61009. https://doi.org/10.1371/journal.pone.0061009 CrossRefPubMedPubMedCentral

Hisasue M, Nagashima N, Nishigaki K, Fukuzawa I, Ura S, Katae H, Tsuchiya R, Yamada T, Hasegawa A, Tsujimoto H (2009) Myelodysplastic syndromes and acute myeloid leukemia in cats infected with Feline leukemia virus clone33 containing a unique long terminal repeat. Int J Cancer 124:1133–1141. https://doi.org/10.1002/ijc.24050 CrossRefPubMed

Hartmann K (2012) Clinical aspects of feline retroviruses: a review. Viruses 4:2684–2710. https://doi.org/10.3390/v4112684 CrossRefPubMedPubMedCentral

Anai Y, Ochi H, Watanabe S, Nakagawa S, Kawamura M, Gojobori T, Nishigaki K (2012) Infectious endogenous retroviruses in cats and emergence of recombinant viruses. J Virol 86:8634–8644. https://doi.org/10.1128/JVI.00280-12 CrossRefPubMedPubMedCentral

Sheets RL, Pandey R, Jen WC, Roy-Burman P (1993) Recombinant feline leukemia virus genes detected in naturally occurring feline lymphosarcomas. J Virol 67:3118–3125PubMedPubMedCentral

Tsatsanis C, Fulton R, Nishigaki K, Tsujimoto H, Levy L, Terry A, Spandidos D, Onions D, Neil JC (1994) Genetic determinants of feline leukemia virus-induced lymphoid tumors: patterns of proviral insertion and gene rearrangement. J Virol 68:8296–8303PubMedPubMedCentral

Nishigaki K, Okuda M, Endo Y, Watari T, Tsujimoto H, Hasegawa A (1997) Structure and function of the long terminal repeats of feline leukemia viruses derived from naturally occurring acute myeloid leukemias in cats. J Virol 71:9823–9827PubMedPubMedCentral

10.

Chandhasin C, Coan PN, Levy LS (2005) Subtle mutational changes in the SU protein of a natural feline leukemia virus subgroup A isolate alter disease spectrum. J Virol 79:1351–1360CrossRef

11.

Miyake A, Watanabe S, Hiratsuka T, Ito J, Ngo MH, Makundi I, Kawasaki J, Endo Y, Tsujimoto H, Nishigaki K (2016) Novel feline leukemia virus interference group based on env gene. J Virol 90:4832–4837. https://doi.org/10.1128/JVI.03229-15 CrossRefPubMedPubMedCentral

12.

Matsumoto Y, Momoi Y, Watari T, Goitsuka R, Tsujimoto H, Hasegawa A (1992) Detection of enhancer repeats in the long terminal repeats of Feline leukemia viruses from cats with spontaneous neoplastic and nonneoplastic diseases. Virology 189:745–749CrossRef

13.

Fulton R, Plumb M, Shield L, Neil JC (1990) Structural diversity and nuclear protein binding sites in the long terminal repeats of Feline leukemia virus. J Virol 64:1675–1682PubMedPubMedCentral

14.

Neil JC, Hughes D, McFarlane R, Wilkie NM, Onions DE, Lees G, Jarrett O (1984) Transduction and rearrangement of the myc gene by feline leukaemia virus in naturally occurring T-cell leukaemias. Nature 308:814–820CrossRef

15.

Levy LS, Gardner MB, Casey JW (1984) Isolation of a feline leukaemia provirus containing the oncogene myc from a feline lymphosarcoma. Nature 308:853–856CrossRef

16.

Mullins JI, Brody DS, Binari RC Jr, Cotter SM (1984) Viral transduction of c-myc gene in naturally occurring feline leukaemias. Nature 308:856–858CrossRef

17.

Fulton R, Forrest D, McFarlane R, Onions D, Neil JC (1987) Retroviral transduction of T-cell antigen receptor beta-chain and myc genes. Nature 326:190–194CrossRef

18.

Rohn JL, Lauring AS, Linenberger ML, Overbaugh J (1996) Transduction of Notch2 in Feline leukemia virus-induced thymic lymphoma. J Virol 70:8071–8080PubMedPubMedCentral

19.

Watanabe S, Ito J, Baba T, Hiratsuka T, Kuse K, Ochi H, Anai Y, Hisasue M, Tsujimoto H, Nishigaki K (2014) Notch2 transduction by Feline leukemia virus in a naturally infected cat. J Vet Med Sci 76:553–557CrossRef

20.

Kawamura M, Umehara D, Odahara Y, Miyake A, Ngo MH, Ohsato Y, Hisasue M, Nakaya MA, Watanabe S, Nishigaki K (2017) AKT capture by feline leukemia virus. Arch Virol 162:1031–1036. https://doi.org/10.1007/s00705-016-3192-1 CrossRefPubMed

21.

Stewart MA, Warnock M, Wheeler A, Wilkie N, Mullins JI, Onions DE, Neil JC (1986) Nucleotide sequences of a feline leukemia virus subgroup A envelope gene and long terminal repeat and evidence for the recombinational origin of subgroup B viruses. J Virol 58:825–834PubMedPubMedCentral

22.

Overbaugh J, Riedel N, Hoover EA, Mullins JI (1988) Transduction of endogenous envelope genes by feline leukaemia virus in vitro. Nature 332:731–734CrossRef

23.

Sheets RL, Pandey R, Jen WC, Roy-Burman P (1993) Recombinant feline leukemia virus genes detected in naturally occurring feline lymphosarcomas. J Virol 67:3118–3125PubMedPubMedCentral

24.

Kawamura M, Watanabe S, Odahara Y, Nakagawa S, Endo Y, Tsujimoto H, Nishigaki K (2015) Genetic diversity in the Feline leukemia virus gag gene. Virus Res 204:74–81. https://doi.org/10.1016/j.virusres.2015.04.008 CrossRefPubMed

25.

Kawasaki J, Kawamura M, Ohsato Y, Ito J, Nishigaki K (2017) Presence of a shared 5’-leader sequence in ancestral human and mammalian retroviruses and its transduction into feline leukemia virus. J Virol 91:e00829-17. https://doi.org/10.1128/JVI.00829-17 CrossRefPubMedPubMedCentral

26.

Forrest D, Onions D, Lees G, Neil JC (1987) Altered structure and expression of c-myc in feline T-cell tumors. Virology 158:194–205CrossRef

27.

Fujino Y, Ohno K, Tsujimoto H (2008) Molecular pathogenesis of feline leukemia virus-induced malignancies: insertional mutagenesis. Vet Immunol Immunopathol 123:138–143. https://doi.org/10.1016/j.vetimm.2008.01.019 CrossRefPubMed

28.

Onions D, Lees G, Forrest D, Neil J (1987) Recombinant feline viruses containing the myc gene rapidly produce clonal tumours expressing T-cell antigen receptor gene transcripts. Int J Cancer 40:40–45CrossRef

29.

Levy LS, Fish RE, Baskin GB (1988) Tumorigenic potential of a myc-containing strain of feline leukemia virus in vivo in domestic cats. J Virol. 62:4770–4773PubMedPubMedCentral

30.

Gil da Costa RM (2015) C-kit as a prognostic and therapeutic marker in canine cutaneous mast cell tumours: From laboratory to clinic. Vet J 205(1):5–10. https://doi.org/10.1016/j.tvjl.2015.05.002 CrossRefPubMed

31.

Braun MJ, Deininger PL, Casey JW (1985) Nucleotide sequence of a transduced myc gene from a defective feline leukemia provirus. J Virol. 55:177–183PubMedPubMedCentral

32.

Stewart MA, Forrest D, McFarlane R, Onions D, Wilkie N, Neil JC (1986) Conservation of the c-myc coding sequence in transduced feline v-myc genes. Virology 154:121–134CrossRef

33.

Doggett DL, Drake AL, Hirsch V, Rowe ME, Stallard V, Mullins JI (1989) Structure, origin, and transforming activity of feline leukemia virus-myc recombinant provirus FTT. J Virol 63:2108–2117PubMedPubMedCentral

34.

Wu FY, Iijima K, Tsujimoto H, Tamura Y, Higurashi M (1995) Chromosomal translocations in two feline T-cell lymphomas. Leuk Res 19:857–860CrossRef

35.

Werner JA, Woo JC, Vernau W, Graham PS, Grahn RA, Lyons LA, Moore PF (2005) Characterization of feline immunoglobulin heavy chain variable region genes for the molecular diagnosis of B-cell neoplasia. Vet Pathol 42:596–607CrossRef

36.

Moore PF, Woo JC, Vernau W, Kosten Graham PS (2005) Characterization of feline T cell receptor gamma (TCRG) variable region genes for the molecular diagnosis of feline intestinal T cell lymphoma. Vet Immunol Immunopathol 106:167–178CrossRef

Title: Polymerase chain reaction-based detection of myc transduction in feline leukemia virus-infected cats
Authors: Ryosuke Sumi
Ariko Miyake
Taiji Endo
Yoshiharu Ohsato
Minh Ha Ngo
Kazuo Nishigaki
Publication date: 01-04-2018
Publisher: Springer Vienna
Published in: Archives of Virology / Issue 4/2018
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-018-3721-1

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Polymerase chain reaction-based detection of myc transduction in feline leukemia virus-infected cats

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2018

Identification and genetic characterization of polyomaviruses in estrildid and fringillid finches

Chromogenic detection of yam mosaic virus by closed-tube reverse transcription loop-mediated isothermal amplification (CT-RT-LAMP)

Physiological traits of endornavirus-infected and endornavirus-free common bean (Phaseolus vulgaris) cv Black Turtle Soup

Detection and analysis of mycovirus-related RNA viruses from grape powdery mildew fungus Erysiphe necator

Enemies with benefits: mutualistic interactions of viruses with lower eukaryotes

Complete genomic sequence of Raphanus sativus cryptic virus 4 (RsCV4), a novel alphapartitivirus from radish

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page