Multiclonal pattern of Jaagsiekte sheep retrovirus integration sites in ovine pulmonary adenocarcinoma

Virus Research

Volumn 117, Issue 2, 2006, Pages 254-263

  Philbey, Adrian W ^a   Cousens, Christina ^a   Bishop, Jeanette V ^b   Gill, Clare A ^c   DeMartini, James C ^b   Sharp, J Michael ^a  

^a MOREDUN RESEARCH INSTITUTE   (United Kingdom)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Integration sites; Jaagsiekte sheep retrovirus; Ovine pulmonary adenocarcinoma; Receptor protein tyrosine phosphatase

Indexed keywords

PROTEIN TYROSINE PHOSPHATASE;

ANIMAL TISSUE; ARTICLE; DNA HYBRIDIZATION; EXON; GENE LOCATION; GENE SEQUENCE; HUMAN; LUNG ADENOCARCINOMA; LUNG TUMOR; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOVIRINAE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; SHEEP; SOUTHERN BLOTTING; TUMOR VOLUME; VIRUS DNA CELL DNA INTERACTION; WALKING;

ANIMALS; BASE SEQUENCE; BLOTTING, SOUTHERN; CHROMOSOMES, MAMMALIAN; DNA; EXONS; JAAGSIEKTE SHEEP RETROVIRUS; KIDNEY; LUNG; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; POLYMERASE CHAIN REACTION; PROTEIN-TYROSINE-PHOSPHATASE; PULMONARY ADENOMATOSIS, OVINE; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; SHEEP; VIRUS INTEGRATION;

ANIMALIA; JAAGSIEKTE SHEEP RETROVIRUS; ONCOVIRINAE; OVIS; OVIS ARIES;

EID: 33646021932     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2005.10.020     Document Type: Article

References (60)

1. Agathanggelou A., Honorio S., Macartney D.P., Martinez A., Dallol A., Rader J., Fullwood P., Chauhan A., Walker R., Shaw J.A., Hosoe S., Lerman M.I., Minna J.D., Maher E.R., and Latif F. Methylation associated inactivation of RASSF1A from region 3p21.3 in lung, breast and ovarian tumors. Oncogene 20 (2001) 1509-1518
2. Aizawa S., Suda Y., Furuta Y., Yagi T., Takeda N., Watanabe N., Nagayoshi M., and Ikawa Y. Env-derived gp55 gene of Friend spleen focus-forming virus specifically induces neoplastic proliferation of erythroid progenitor cells. EMBO J. 9 (1990) 2107-2116
3. Alberti A., Murgia C., Liu S.-L., Mura M., Cousens C., Sharp M., Miller A.D., and Palmarini M. Envelope-induced cell transformation by ovine betaretroviruses. J. Virol. 76 (2002) 5387-5394
4. Alian A., Sela-Donenfeld D., Panet A., and Eldor A. Avian hemangioma retrovirus induces cell proliferation via the envelope (env) gene. Virology 276 (2000) 161-168
5. Allen T.E., Sherrill K.J., Crispell S.M., Perrott M.R., Carlson J.O., and DeMartini J.C. The Jaagsiekte sheep retrovirus envelope gene induces transformation of the avian fibroblast cell line DF-1 but does not require a conserved SH2 binding domain. J. Gen. Virol. 83 (2002) 2733-2742
6. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
7. Aoyagi Y., Yokose T., Minami Y., Ochiai A., Iijima T., Morishita Y., Oda T., Fukao K., and Noguchi M. Accumulation of losses of heterozygosity and multistep carcinogenesis in pulmonary adenocarcinoma. Cancer Res. 61 (2001) 7950-7954
8. Bai J., Bishop J.V., Carlson J.O., and DeMartini J.C. Sequence comparison of JSRV with endogenous proviruses: envelope genotypes and a novel ORF with similarity to a G-protein-coupled receptor. Virology 258 (1999) 333-343
9. Bai J., Zhu R.Y., Stedman K., Cousens C., Carlson J., Sharp J.M., and DeMartini J.C. Unique long terminal repeat U3 sequences distinguish exogenous Jaagsiekte sheep retroviruses associated with ovine pulmonary carcinoma from endogenous loci in the sheep genome. J. Virol. 70 (1996) 3159-3168
10. Barsky S.H., Grossman D.A., Ho J., and Holmes E.C. The multifocality of bronchioloalveolar lung carcinoma: evidence and implications of a multiclonal origin. Mod. Pathol. 7 (1994) 633-640
11. Burkin D.J., Broad T.E., Lambeth M.R., Burkin H.R., and Jones C. New gene assignments using a complete, characterized sheep-hamster somatic cell hybrid panel. Anim. Genet. 29 (1998) 48-54
12. Carlson J., Lyon M., Bishop J., Vaiman A., Cribiu E., Mornex J.F., Brown S., Knudson D., DeMartini J., and Leroux C. Chromosomal distribution of endogenous Jaagsiekte sheep retrovirus proviral sequences in the sheep genome. J. Virol. 77 (2003) 9662-9668
13. Cho B.C., Shaughnessy Jr. J.D., Largaespada D.A., Bedigian H.G., Buchberg A.M., Jenkins N.A., and Copeland N.G. Frequent disruption of the Nf1 gene by a novel murine AIDS virus-related provirus in BXH-2 murine myeloid lymphomas. J. Virol. 69 (1995) 7138-7146
14. Cousens C., Bishop J.V., Philbey A.W., Gill C.A., Palmarini M., Carlson J.O., DeMartini J.C., and Sharp J.M. Analysis of integration sites of Jaagsiekte sheep retrovirus in ovine pulmonary adenocarcinoma. J. Virol. 78 (2004) 8506-8512
15. Danilkovitch-Miagkova A., Duh F.M., Kuzmin I., Angeloni D., Liu S.L., Miller A.D., and Lerman M.I. Hyaluronidase 2 negatively regulates RON receptor tyrosine kinase and mediates transformation of epithelial cells by Jaagsiekte sheep retrovirus. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 4580-4585
16. DeMartini J.C., Bishop J.V., Allen T.E., Jassim F.A., Sharp J.M., De las Heras M., Voelker D.R., and Carlson J.O. Jaagsiekte sheep retrovirus proviral clone JSRV (JS7), derived from the JS7 lung tumor cell line, induces ovine pulmonary carcinoma and is integrated into the surfactant protein A gene. J. Virol. 75 (2001) 4239-4246
17. Don R.H., Cox P.T., Wainwright B.J., Baker K., and Mattick J.S. 'Touchdown' PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res. 19 (1991) 4008
18. Dreijerink K., Braga E., Kuzmin I., Geil L., Duh F.M., Angeloni D., Zbar B., Lerman M.I., Stanbridge E.J., Minna J.D., Protopopov A., Li J., Kashuba V., Klein G., and Zabarovsky E.R. The candidate tumor suppressor gene, RASSF1A, from human chromosome 3p21.3 is involved in kidney tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 7504-7509
19. Gill C.A., Davis S.K., Taylor J.F., Cockett N.E., and Bottema C.D.K. Construction and characterization of an ovine bacterial artificial chromosome library. Mamm. Genome 10 (1999) 1108-1111
20. Hicks G.G., and Mowat M. Integration of Friend murine leukemia virus into both alleles of the p53 oncogene in an erythroleukemic cell line. J. Virol. 62 (1988) 4752-4755
21. Holland M.J., Palmarini M., Garcia-Goti M., Gonzalez L., McKendrick I., De las Heras M., and Sharp J.M. Jaagsiekte retrovirus is widely distributed both in T and B lymphocytes and in mononuclear phagocytes of sheep with naturally and experimentally acquired pulmonary adenomatosis. J. Virol. 73 (1999) 4004-4008
22. Kastury K., Ohta M., Lasota J., Moir D., Dorman T., LaForgia S., Druck T., and Huebner K. Structure of the human receptor tyrosine phosphatase gamma gene (PTPRG) and relation to the familial RCC t(3;8) chromosome translocation. Genomics 32 (1996) 225-235
23. Kok K., Osinga J., Carritt B., Davis M.B., van der Hout A.H., van der Veen A.Y., Landsvater R.M., de Leij L.F.M.H., Berendsen H.H., Postmus P.E., Poppema S., and Buys C.H.C.M. Deletion of a DNA sequence at the chromosomal region 3p21 in all major types of lung cancer. Nature 330 (1987) 578-581
24. Kovacs G., Erlandsson R., Boldog F., Ingvarsson S., Müller-Brechlin R., Klein G., and Sümegi J. Consistent chromosome 3p deletion and loss of heterozygosity in renal cell carcinoma. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 1571-1575
25. LaForgia S., Lasota J., Latif F., Boghosian-Sell L., Kastury K., Ohta M., Druck T., Atchison L., Cannizzaro L.A., Barnea G., Schlessinger J., Modi W., Kuzmin I., Tory K., Zbar B., Croce C.M., Lerman M., and Huebner K. Detailed genetic and physical map of the 3p chromosome region surrounding the familial renal cell carcinoma chromosome translocation, t(3;8)(p14.2;q24.1). Cancer Res. 53 (1993) 3118-3124
26. LaForgia S., Morse B., Levy J., Barnea G., Cannizzaro L.A., Li F., Nowell P.C., Boghosian-Sell L., Glick J., Weston A., Harris C.C., Drabkin H., Patterson D., Croce C.E., Schlessinger J., and Huebner K. Receptor protein-tyrosine phosphatase gamma is a candidate tumor suppressor gene at human chromosome region 3p21. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 5036-5040
27. Leclercq I., Cavrois M., Mortreux F., Hermine O., Gessain A., Morschhauser F., and Wattel E. Oligoclonal proliferation of human T-cell leukaemia virus type 1 bearing T cells in adult T-cell leukaemia/lymphoma without deletion of the 3′ provirus integration sites Br. J. Haematol. 101 (1998) 500-506
28. Lerman M.I., and Minna J.D. The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: identification and evaluation of the resident candidate tumor suppressor genes. The International Lung Cancer Chromosome 3p21. 3 Tumor Suppressor Gene Consortium. Cancer Res. 60 (2000) 6116-6133
29. Liu S.L., Lerman M.I., and Miller A.D. Putative phosphatidylinositol 3-kinase (PI3K) binding motifs in ovine betaretrovirus Env proteins are not essential for rodent fibroblast transformation and PI3K/Akt activation. J. Virol. 77 (2003) 7924-7935
30. Lu S.J., Rowan S., Bani M.R., and Ben-David Y. Retroviral integration within the Fli-2 locus results in inactivation of the erythroid transcription factor NF-E2 in Friend erythroleukemias: evidence that NF-E2 is essential for globin expression. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 8398-8402
31. Maeda N., Fu W., Ortin A., de las Heras M., and Fan H. Roles of the Ras-MEK-mitogen-activated protein kinase and phosphatidylinositol 3-kinase-Akt-mTOR pathways in Jaagsiekte sheep retrovirus-induced transformation of rodent fibroblast and epithelial cell lines. J. Virol. 79 (2005) 4440-4450
32. Maeda N., Inoshima Y., Fruman D.A., Brachmann S.M., and Fan H. Transformation of mouse fibroblasts by Jaagsiekte sheep retrovirus envelope does not require phosphatidylinositol 3-kinase. J. Virol. 77 (2003) 9951-9959
33. Maeda N., Palmarini M., Murgia C., and Fan H. Direct transformation of rodent fibroblasts by Jaagsiekte sheep retrovirus DNA. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 4449-4454
34. Moscow J.A., He R., Gnarra J.R., Knutsen T., Weng Y., Zhao W.P., Whang-Peng J., Linehan W.M., and Cowan K.H. Examination of human tumors for rhoA mutations. Oncogene 9 (1994) 189-194
35. Niho S., Yokose T., Suzuki K., Kodama T., Nishiwaki Y., and Mukai K. Monoclonality of atypical adenomatous hyperplasia of the lung. Am. J. Pathol. 154 (1999) 249-254
36. Ortín A., Minguijón E., Dewar P., Garcia M., Ferrer L.M., Palmarini M., Gonzalez L., Sharp J.M., and De las Heras M. Lack of a specific immune response against a recombinant capsid protein of Jaagsiekte sheep retrovirus in sheep and goats naturally affected by enzootic nasal tumor or sheep pulmonary adenomatosis. Vet. Immunol. Immunopathol. 61 (1998) 229-237
37. Palmarini M., Cousens C., Dalziel R.G., Bai J., Stedman K., DeMartini J.C., and Sharp J.M. The exogenous form of Jaagsiekte retrovirus is specifically associated with a contagious lung cancer of sheep. J. Virol. 70 (1996) 1618-1623
38. Palmarini M., Datta S., Omid R., Murgia C., and Fan H. The long terminal repeat of Jaagsiekte sheep retrovirus is preferentially active in differentiated epithelial cells of the lungs. J. Virol. 74 (2000) 5776-5787
39. Palmarini M., and Fan H. Retrovirus-induced ovine pulmonary adenocarcinoma, an animal model for lung cancer. J. Natl. Cancer Inst. 93 (2001) 1603-1614
40. Palmarini M., Maeda N., Murgia C., De-Fraja C., Hofacre A., and Fan H. A phosphatidylinositol 3-kinase docking site in the cytoplasmic tail of the Jaagsiekte sheep retrovirus transmembrane protein is essential for envelope-induced transformation of NIH 3T3 cells. J. Virol. 75 (2001) 11002-11009
41. Palmarini M., Mura M., and Spencer T.E. Endogenous betaretroviruses of sheep: teaching new lessons in retroviral interference and adaptation. J. Gen. Virol. 85 (2004) 1-13
42. Palmarini M., Sharp J.M., De las Heras M., and Fan H. Jaagsiekte sheep retrovirus is necessary and sufficient to induce a contagious lung cancer in sheep. J. Virol. 73 (1999) 6964-6972
43. Poirier Y., Kozak C., and Jolicoeur P. Identification of a common helper provirus integration site in Abelson murine leukemia virus-induced lymphoma DNA. J. Virol. 62 (1988) 3985-3992
44. Rai S.K., DeMartini J.C., and Miller A.D. Retrovirus vectors bearing Jaagsiekte sheep retrovirus Env transduce human cells by using a new receptor localized to chromosome 3p21.3. J. Virol. 74 (2000) 4698-4704
45. Rai S.K., Duh F.M., Vigdorovich V., Danilkovitch-Miagkova A., Lerman M.I., and Miller A.D. Candidate tumor suppressor HYAL2 is a glycosylphosphatidylinositol (GPI)-anchored cell-surface receptor for Jaagsiekte sheep retrovirus, the envelope protein of which mediates oncogenic transformation. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 4443-4448
46. Rimessi P., Gualandi F., Morelli C., Trabanelli C., Wu Q., Possati L., Montesi M., Barrett J.C., and Barbanti-Brodano G. Transfer of human chromosome 3 to an ovarian carcinoma cell line identifies three regions on 3p involved in ovarian cancer. Oncogene 9 (1994) 3467-3474
47. Rosati S., Pittau M., Alberti A., Pozzi S., York D.F., Sharp J.M., and Palmarini M. An accessory open reading frame (orf-x) of Jaagsiekte sheep retrovirus is conserved between different virus isolates. Virus Res. 66 (2000) 109-116
48. Sarkar N.H. Clonal variations among multiple primary mammary tumors and within a tumor of individual mice: insertion mutations of int oncogenes. Virology 212 (1995) 490-499
49. Sharp J.M., and DeMartini J.C. Natural history of JSRV in sheep. Curr. Top. Microbiol. Immunol. 275 (2003) 55-79
50. Schibler L., Vaiman D., Oustry A., Giraud-Delville C., and Cribiu E.P. Comparative gene mapping: a fine-scale survey of chromosome rearrangements between ruminants and humans. Genome Res. 8 (1998) 901-915
51. Shin S.W., Breathnach O.S., Linnoila R.I., Williams J., Gillespie J.W., Kelley M.J., and Johnson B.E. Genetic changes in contralateral bronchioloalveolar carcinomas of the lung. Oncology 60 (2001) 81-87
52. Sithanandam G., Latif F., Duh F.M., Bernal R., Smola U., Li H., Kuzmin I., Wixler V., Geil L., Shrestha S., Lloyd P.A., Bader S., Sekido Y., Tartof K.D., Kashuba V.I., Zabarovsky E.R., Dean M., Klein G., Zbar B., Lerman M.I., Minna J.D., Rapp U.R., and Allikmets A. 3pK, a new mitogen-activated protein kinase-activated protein kinase located in the small cell lung cancer tumor suppressor gene region. Mol. Cell Biol. 16 (1996) 868-876
53. Sozzi G., Veronese M.L., Negrini M., Baffa R., Cotticelli M.G., Inoue H., Tornielli S., Pilotti S., De Gregorio L., Pastorino U., Pierotti M.A., Ohta M., Huebner K., and Croce C.M. The FHIT gene 3p14.2 is abnormal in lung cancer. Cell 85 (1996) 17-26
54. Szeles A., Bajalica-Lagercrantz S., Lindblom A., Lushnikova T., Kashuba V.I., Imreh S., Nordenskjold M., Klein G., and Zabarovsky E.R. Mapping of a new MAP kinase activated protein kinase gene (3PK) to human chromosome band 3p21.2 and ordering of 3PK and two cosmid markers in the 3p22-p21 tumor-suppressor region by two-colour fluorescence in situ hybridization. Chromosome Res. 4 (1996) 310-313
55. Tai T.C., Lye S.J., and Adamson S.L. Expression of prostaglandin E2 receptor subtypes in the developing sheep brainstem. Brain Res. Mol. Brain Res. 57 (1998) 161-166
56. Tsukamoto T., Takahashi T., Ueda R., Hibi K., Saito H., and Takahashi T. Molecular analysis of the protein tyrosine phosphatase gamma gene in human lung cancer cell lines. Cancer Res. 52 (1992) 3506-3509
57. Wary K.K., Lou Z., Buchberg A.M., Siracusa L.D., Druck T., LaForgia S., and Huebner K. A homozygous deletion within the carbonic anhydrase-like domain of the Ptprg gene in murine L-cells. Cancer Res. 53 (1993) 1498-1502
58. Wootton S.K., Halbert C.L., and Miller A.D. Sheep retrovirus structural protein induces lung tumors. Nature 434 (2005) 904-907
59. York D.F., Vigne R., Verwoerd D.W., and Querat G. Nucleotide sequence of the Jaagsiekte retrovirus, an exogenous and endogenous type D and B retrovirus of sheep and goats. J. Virol. 66 (1992) 4930-4939
60. Zavala G., Pretto C., Chow Y.H., Jones L., Alberti A., Grego E., De las Heras M., and Palmarini M. Relevance of Akt phosphorylation in cell transformation induced by Jaagsiekte sheep retrovirus. Virology 312 (2003) 95-105