Biopolym. Cell. 1998; 14(4):286-297.
Регіональна специфічність вірусної інтеграції
1Риндич А. В., 1Зубак С. В., 1Циба Л. О., 1Гулей Н., 1Лазуркевич З. В., 2Бернарді Дж.
  1. Інститут молекулярної біології і генетики НАН України
    Вул. Академіка Заболотного, 150, Київ, Україна, 03680
  2. Інститут Жак Моно, CNRS-Університет Париж VII,
    2, Жусье, Париж, Франція, 75005

Abstract

Інтеграція ретровірусів у геном хазяїв до недавнього часу вважалася випадковою і на сьогодні не існує ясності, як впливають виявлені в місцях встановлених локальних ефектів в місцях інтеграції локальні ефекти на процес інтеграції в цілий геном. Використання композиційного підходу дало можливість встановити, що інтеграція ретровірусів відбувається у певні райони геному, які тотожні вірусним послідовностям за складом основ. Цю регіональну специфічність інтеграції доведено: 1) нашими експериментальними даними з локалізації ретровірусних послідовностей у різних композиційних ділянках геному; 2) результатами з інших лабораторій стосовно локалізації ретровірусних послідовностей у «відкритих» ділянках хроматину або/чи біля СрG-«острівців»; 3) нашим композиційним аналізом генів, розташованих по сусідству з інтегрованими вірусними послідовностями. Такий висновок має значення як для розуміння композиційної еволюції ретровірусних геномів, так і для генної терапії.

References

[1] Temin HM. The DNA provirus hypothesis. Science. 1976;192(4244):1075-80.
[2] Varmus HE. The molecular genetics of cellular oncogenes. Annu Rev Genet. 1984;18:553-612.
[3] Goff SP. Genetics of retroviral integration. Annu Rev Genet. 1992;26:527-44.
[4] Kung HJ, Boerkoel C, Carter TH. Retroviral mutagenesis of cellular oncogenes: a review with insights into the mechanisms of insertional activation. Curr Top Microbiol Immunol. 1991;171:1-25.
[5] Tsichlis PN, Lazo PA. Virus-host interactions and the pathogenesis of murine and human oncogenic retroviruses. Curr Top Microbiol Immunol. 1991;171:95-171.
[6] Athas GB, Starkey CR, Levy LS. Retroviral determinants of leukemogenesis. Crit Rev Oncog. 1994;5(2-3):169-99.
[7] Jonkers J, Berns A. Retroviral insertional mutagenesis as a strategy to identify cancer genes. Biochim Biophys Acta. 1996;1287(1):29-57.
[8] Largaespada DA, Shaughnessy JD Jr, Jenkins NA, Copeland NG. Retroviral integration at the Evi-2 locus in BXH-2 myeloid leukemia cell lines disrupts Nf1 expression without changes in steady-state Ras-GTP levels. J Virol. 1995;69(8):5095-102.
[9] Shen-Ong GL, Morse HC 3rd, Potter M, Mushinski JF. Two modes of c-myb activation in virus-induced mouse myeloid tumors. Mol Cell Biol. 1986;6(2):380-92.
[10] Weinstein Y, Cleveland JL, Askew DS, Rapp UR, Ihle JN. Insertion and truncation of c-myb by murine leukemia virus in a myeloid cell line derived from cultures of normal hematopoietic cells. J Virol. 1987;61(7):2339-43.
[11] Setoguchi M, Higuchi Y, Yoshida S, Nasu N, Miyazaki Y, Akizuki S, Yamamoto S. Insertional activation of N-myc by endogenous Moloney-like murine retrovirus sequences in macrophage cell lines derived from myeloma cell line-macrophage hybrids. Mol Cell Biol. 1989;9(10):4515-22.
[12] Bishop JM. Enemies within: the genesis of retrovirus oncogenes. Cell. 1981;23(1):5-6.
[13] Neil JC. Defective avian sarcoma viruses. Curr Top Microbiol Immunol. 1983;103:51-74.
[14] Hughes SH. Synthesis, integration, and transcription of the retroviral provirus. Curr Top Microbiol Immunol. 1983;103:23-49.
[15] Bushman F. Targeting retroviral integration. Science. 1995;267(5203):1443-4.
[16] Anderson WF. Human gene therapy. Nature. 1998;392(6679 Suppl):25-30.
[17] Varmus HE, Brown P. Retroviruses. Mobile DNA American Society for Microbiology. Eds D. E. Berg, M. M. Howe. Washington: DC, 1989: 53-108.
[18] Grandgenett DP, Mumm SR. Unraveling retrovirus integration. Cell. 1990;60(1):3-4. PubMed PMID: 6250443.
[19] Weinberg RA. Integrated genomes of animal viruses. Annu Rev Biochem. 1980;49:197-226.
[20] Hayward WS, Neel BG, Astrin SM. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981;290(5806):475-80.
[21] Payne GS, Bishop JM, Varmus HE. Multiple arrangements of viral DNA and an activated host oncogene in bursal lymphomas. Nature. 1982;295(5846):209-14.
[22] Brown PO, Bowerman B, Varmus HE, Bishop JM. Correct integration of retroviral DNA in vitro. Cell. 1987;49(3):347-56.
[23] Fujiwara T, Mizuuchi K. Retroviral DNA integration: structure of an integration intermediate. Cell. 1988;54(4):497-504.
[24] Withers-Ward ES, Kitamura Y, Barnes JP, Coffin JM. Distribution of targets for avian retrovirus DNA integration in vivo. Genes Dev. 1994;8(12):1473-87.
[25] Filipski J, Thiery JP, Bernardi G. An analysis of the bovine genome by Cs2SO4-Ag density gradient centrifugation. J Mol Biol. 1973;80(1):177-97.
[26] Thiery JP, Macaya G, Bernardi G. An analysis of eukaryotic genomes by density gradient centrifugation. J Mol Biol. 1976;108(1):219-35.
[27] Macaya G, Thiery JP, Bernardi G. An approach to the organization of eukaryotic genomes at a macromolecular level. J Mol Biol. 1976;108(1):237-54.
[28] Kettmann R, Meunier-Rotival M, Cortadas J, Cuny G, Ghysdael J, Mammerickx M, Burny A, Bernardi G. Integration of bovine leukemia virus DNA in the bovine genome. Proc Natl Acad Sci U S A. 1979;76(10):4822-6.
[29] De Sario A, Roizes G, Allegre N, Bernardi G. A compositional map of the cen-q21 region of human chromosome 21. Gene. 1997;194(1):107-13.
[30] Bernardi G. The human genome: organization and evolutionary history. Annu Rev Genet. 1995;29:445-76.
[31] Sabeur G, Macaya G, Kadi F, Bernardi G. The isochore patterns of mammalian genomes and their phylogenetic implications. J Mol Evol. 1993;37(2):93-108.
[32] Zoubak S, Clay O, Bernardi G. The gene distribution of the human genome. Gene. 1996;174(1):95-102.
[33] Bernardi G, Bernardi G. Compositional constraints and genome evolution. J Mol Evol. 1986;24(1-2):1-11.
[34] Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G, Meunier-Rotival M, Rodier F. The mosaic genome of warm-blooded vertebrates. Science. 1985;228(4702):953-8.
[35] Clay O, Cacci? S, Zoubak S, Mouchiroud D, Bernardi G. Human coding and noncoding DNA: compositional correlations. Mol Phylogenet Evol. 1996;5(1):2-12.
[36] Mouchiroud D, D'Onofrio G, A?ssani B, Macaya G, Gautier C, Bernardi G. The distribution of genes in the human genome. Gene. 1991;100:181-7.
[37] Saccone S, Caccio S, Perani P, Andreozzi L, Rapisarda A, Motta S, Bernardi G. Compositional mapping of mouse chromosomes and identification of the gene-rich regions. Chromosome Res. 1997;5(5):293-300.
[38] Saccone S, De Sario A, Della Valle G, Bernardi G. The highest gene concentrations in the human genome are in telomeric bands of metaphase chromosomes. Proc Natl Acad Sci U S A. 1992;89(11):4913-7.
[39] Sorry, this reference was missed last century
[40] Tazi J, Bird A. Alternative chromatin structure at CpG islands. Cell. 1990;60(6):909-20.
[41] Kettmann R, Cleuter Y, Mammerickx M, Meunier-Rotival M, Bernardi G, Burny A, Chantrenne H. Genomic integration of bovine leukemia provirus: comparison of persistent lymphocytosis with lymph node tumor form of enzootic. Proc Natl Acad Sci U S A. 1980;77(5):2577-81.
[42] Zoubak S, Richardson JH, Rynditch A, H?llsberg P, Hafler DA, Boeri E, Lever AM, Bernardi G. Regional specificity of HTLV-I proviral integration in the human genome. Gene. 1994;143(2):155-63.
[43] Rynditch A, Kadi F, Geryk J, Zoubak S, Svoboda J, Bernardi G. The isopycnic, compartmentalized integration of Rous sarcoma virus sequences. Gene. 1991;106(2):165-72.
[44] Salinas J, Zerial M, Filipski J, Crepin M, Bernardi G. Nonrandom distribution of MMTV proviral sequences in the mouse genome. Nucleic Acids Res. 1987;15(7):3009-22.
[45] Bodor J, Svoboda J. The LTR, v-src, LTR provirus generated in the mammalian genome by src mRNA reverse transcription and integration. J Virol. 1989;63(2):1015-8.
[46] Machon O, Hejnar J, H?jkov? P, Geryk J, Svoboda J. The LTR, v-src, LTR provirus in H-19 hamster tumor cell line is integrated adjacent to the negative regulatory region. Gene. 1996;174(1):9-17.
[47] Salinas J, Zerial M, Filipski J, Bernardi G. Gene distribution and nucleotide sequence organization in the mouse genome. Eur J Biochem. 1986;160(3):469-78.
[48] Zerial M, Salinas J, Filipski J, Bernardi G. Genomic localization of hepatitis B virus in a human hepatoma cell line. Nucleic Acids Res. 1986;14(21):8373-86.
[49] Romani M, Casciano I, Querzola F, De Ambrosis A, Siniscalco M. Analysis of a viral integration event in a CG-rich region at the 1p36 human chromosomal site. Gene. 1993;135(1-2):153-60.
[50] Marcus SL, Smith SW, Sarkar NH. Quantitative of murine mammary tumor virus-related RNA in mammary tissues of low- and high-mammary-tumor-incidence mouse strains. J Virol. 1981;40(1):87-95.
[51] Choi YW, Henrard D, Lee I, Ross SR. The mouse mammary tumor virus long terminal repeat directs expression in epithelial and lymphoid cells of different tissues in transgenic mice. J Virol. 1987;61(10):3013-9.
[52] Henrard D, Ross SR. Endogenous mouse mammary tumor virus is expressed in several organs in addition to the lactating mammary gland. J Virol. 1988;62(8):3046-9.
[53] Vijaya S, Steffen DL, Robinson HL. Acceptor sites for retroviral integrations map near DNase I-hypersensitive sites in chromatin. J Virol. 1986;60(2):683-92.
[54] Rohdewohld H, Weiher H, Reik W, Jaenisch R, Breindl M. Retrovirus integration and chromatin structure: Moloney murine leukemia proviral integration sites map near DNase I-hypersensitive sites. J Virol. 1987;61(2):336-43.
[55] Scherdin U, Rhodes K, Breindl M. Transcriptionally active genome regions are preferred targets for retrovirus integration. J Virol. 1990;64(2):907-12.
[56] Mooslehner K, Karls U, Harbers K. Retroviral integration sites in transgenic Mov mice frequently map in the vicinity of transcribed DNA regions. J Virol. 1990;64(6):3056-8.
[57] Fincham VJ, Wyke JA. Differences between cellular integration sites of transcribed and nontranscribed Rous sarcoma proviruses. J Virol. 1991;65(1):461-3.
[58] Robinson HL, Gagnon GC. Patterns of proviral insertion and deletion in avian leukosis virus-induced lymphomas. J Virol. 1986;57(1):28-36.
[59] Schubach W, Groudine M. Alteration of c-myc chromatin structure by avian leukosis virus integration. Nature. 1984 Feb 23-29;307(5953):702-8.
[60] Edmondson DG, Roth SY. Chromatin and transcription. FASEB J. 1996;10(10):1173-82.
[61] A?ssani B, Bernardi G. CpG islands, genes and isochores in the genomes of vertebrates. Gene. 1991;106(2):185-95.
[62] A?ssani B, Bernardi G. CpG islands: features and distribution in the genomes of vertebrates. Gene. 1991;106(2):173-83.
[63] Ozturk M. Chromosomal rearrangements and tumor suppressor genes in primary liver cancer. Primary liver cancer: etiological and progression factors. Ed. C. Brechat. Boca Raton: CRC press, 1994: 269-81.
[64] Lazo PA, Lee JS, Tsichlis PN. Long-distance activation of the Myc protooncogene by provirus insertion in Mlvi-1 or Mlvi-4 in rat T-cell lymphomas. Proc Natl Acad Sci U S A. 1990;87(1):170-3.
[65] Bartholomew C, Ihle JN. Retroviral insertions 90 kilobases proximal to the Evi-1 myeloid transforming gene activate transcription from the normal promoter. Mol Cell Biol. 1991;11(4):1820-8.
[66] Jiang X, Villeneuve L, Turmel C, Kozak CA, Jolicoeur P. The Myb and Ahi-1 genes are physically very closely linked on mouse chromosome 10. Mamm Genome. 1994;5(3):142-8.
[67] Shen-Ong GL, Wolff L. Moloney murine leukemia virus-induced myeloid tumors in adult BALB/c mice: requirement of c-myb activation but lack of v-abl involvement. J Virol. 1987;61(12):3721-5.
[68] Wolff L, Koller R, Davidson W. Acute myeloid leukemia induction by amphotropic murine retrovirus (4070A): clonal integrations involve c-myb in some but not all leukemias. J Virol. 1991;65(7):3607-16.
[69] Bordereaux D, Fichelson S, Sola B, Tambourin PE, Gisselbrecht S. Frequent involvement of the fim-3 region in Friend murine leukemia virus-induced mouse myeloblastic leukemias. J Virol. 1987;61(12):4043-5.
[70] Mushinski JF, Mountz JD, Pierce JH, Pumphrey JG, Skurla RM Jr, Finkelman FD, Givol D, Davidson WF. Expression of the murine proto-oncogene bcl-2 is stage specific and cell-type specific. Curr Top Microbiol Immunol. 1988;141:332-6.
[71] Morishita K, Parker DS, Mucenski ML, Jenkins NA, Copeland NG, Ihle JN. Retroviral activation of a novel gene encoding a zinc finger protein in IL-3-dependent myeloid leukemia cell lines. Cell. 1988;54(6):831-40.
[72] Pachl C, Schubach W, Eisenman R, Linial M. Expression of c-myc RNA in bursal lymphoma cell lines: identification of c-myc-encoded proteins by hybrid-selected translation. Cell. 1983;33(2):335-44.
[73] Boerkoel CF, Kung HJ. Transcriptional interaction between retroviral long terminal repeats (LTRs): mechanism of 5' LTR suppression and 3' LTR promoter activation of c-myc in avian B-cell lymphomas. J Virol. 1992;66(8):4814-23.
[74] Fung YK, Lewis WG, Crittenden LB, Kung HJ. Activation of the cellular oncogene c-erbB by LTR insertion: molecular basis for induction of erythroblastosis by avian leukosis virus. Cell. 1983;33(2):357-68.
[75] Nilsen TW, Maroney PA, Goodwin RG, Rottman FM, Crittenden LB, Raines MA, Kung HJ. c-erbB activation in ALV-induced erythroblastosis: novel RNA processing and promoter insertion result in expression of an amino-truncated EGF receptor. Cell. 1985;41(3):719-26.
[76] Collart KL, Aurigemma R, Smith RE, Kawai S, Robinson HL. Infrequent involvement of c-fos in avian leukosis virus-induced nephroblastoma. J Virol. 1990;64(7):3541-4.
[77] Kabrun N, Bumstead N, Hayman MJ, Enrietto PJ. Characterization of a novel promoter insertion in the c-rel locus. Mol Cell Biol. 1990;10(9):4788-94.
[78] Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell. 1982;31(1):99-109.
[79] Peters G, Brookes S, Smith R, Placzek M, Dickson C. The mouse homolog of the hst/k-FGF gene is adjacent to int-2 and is activated by proviral insertion in some virally induced mammary tumors. Proc Natl Acad Sci U S A. 1989;86(15):5678-82.
[80] Morris DW, Dutra JC. Identification of a MMTV insertion mutation within the coding region of the Fgf-3 protooncogene. Virology. 1997;238(1):161-5.
[81] Gallahan D, Callahan R. Mammary tumorigenesis in feral mice: identification of a new int locus in mouse mammary tumor virus (Czech II)-induced mammary tumors. J Virol. 1987;61(1):66-74.
[82] Roelink H, Wagenaar E, Lopes da Silva S, Nusse R. Wnt-3, a gene activated by proviral insertion in mouse mammary tumors, is homologous to int-1/Wnt-1 and is normally expressed in mouse embryos and adult brain. Proc Natl Acad Sci U S A. 1990;87(12):4519-23.
[83] Peters G, Brookes S, Placzek M, Schuermann M, Michalides R, Dickson C. A putative int domain for mouse mammary tumor virus on mouse chromosome 7 is a 5' extension of int-2. J Virol. 1989;63(3):1448-50.
[84] MacArthur CA, Shankar DB, Shackleford GM. Fgf-8, activated by proviral insertion, cooperates with the Wnt-1 transgene in murine mammary tumorigenesis. J Virol. 1995;69(4):2501-7.
[85] Marchetti A, Buttitta F, Miyazaki S, Gallahan D, Smith GH, Callahan R. Int-6, a highly conserved, widely expressed gene, is mutated by mouse mammary tumor virus in mammary preneoplasia. J Virol. 1995;69(3):1932-8.
[86] Lee FS, Lane TF, Kuo A, Shackleford GM, Leder P. Insertional mutagenesis identifies a member of the Wnt gene family as a candidate oncogene in the mammary epithelium of int-2/Fgf-3 transgenic mice. Proc Natl Acad Sci U S A. 1995;92(6):2268-72.
[87] Morris DW, Barry PA, Bradshaw HD Jr, Cardiff RD. Insertion mutation of the int-1 and int-2 loci by mouse mammary tumor virus in premalignant and malignant neoplasms from the GR mouse strain. J Virol. 1990;64(4):1794-802.
[88] Dickson C, Smith R, Brookes S, Peters G. Proviral insertions within the int-2 gene can generate multiple anomalous transcripts but leave the protein-coding domain intact. J Virol. 1990;64(2):784-93.
[89] Miyazaki S, Kozak CA, Marchetti A, Buttitta F, Gallahan D, Callahan R. The chromosomal location of the mouse mammary tumor gene Int6 and related pseudogenes in the mouse genome. Genomics. 1995;27(3):420-4.
[90] Robbins J, Blondel BJ, Gallahan D, Callahan R. Mouse mammary tumor gene int-3: a member of the notch gene family transforms mammary epithelial cells. J Virol. 1992;66(4):2594-9.
[91] Diella F, Levi G, Callahan R. Characterization of the INT6 mammary tumor gene product. DNA Cell Biol. 1997;16(7):839-47.
[92] Pryciak PM, Varmus HE. Nucleosomes, DNA-binding proteins, and DNA sequence modulate retroviral integration target site selection. Cell. 1992;69(5):769-80.
[93] Pryciak PM, Sil A, Varmus HE. Retroviral integration into minichromosomes in vitro. EMBO J. 1992;11(1):291-303.
[94] Pryciak PM, M?ller HP, Varmus HE. Simian virus 40 minichromosomes as targets for retroviral integration in vivo. Proc Natl Acad Sci U S A. 1992;89(19):9237-41.
[95] Kitamura Y, Lee YM, Coffin JM. Nonrandom integration of retroviral DNA in vitro: effect of CpG methylation. Proc Natl Acad Sci U S A. 1992;89(12):5532-6.
[96] M?ller HP, Varmus HE. DNA bending creates favored sites for retroviral integration: an explanation for preferred insertion sites in nucleosomes. EMBO J. 1994;13(19):4704-14.
[97] Pruss D, Bushman FD, Wolffe AP. Human immunodeficiency virus integrase directs integration to sites of severe DNA distortion within the nucleosome core. Proc Natl Acad Sci U S A. 1994;91(13):5913-7.
[98] Bor YC, Bushman FD, Orgel LE. In vitro integration of human immunodeficiency virus type 1 cDNA into targets containing protein-induced bends. Proc Natl Acad Sci U S A. 1995;92(22):10334-8.
[99] Chou KS, Okayama A, Su IJ, Lee TH, Essex M. Preferred nucleotide sequence at the integration target site of human T-cell leukemia virus type I from patients with adult T-cell leukemia. Int J Cancer. 1996;65(1):20-4.
[100] Shimotohno K, Temin HM. No apparent nucleotide sequence specificity in cellular DNA juxtaposed to retrovirus proviruses. Proc Natl Acad Sci U S A. 1980;77(12):7357-61.
[101] Meunier-Rotival M, Soriano P, Cuny G, Strauss F, Bernardi G. Sequence organization and genomic distribution of the major family of interspersed repeats of mouse DNA. Proc Natl Acad Sci U S A. 1982;79(2):355-9.
[102] Peckham I, Sobel S, Comer J, Jaenisch R, Barklis E. Retrovirus activation in embryonal carcinoma cells by cellular promoters. Genes Dev. 1989;3(12B):2062-71.
[103] Zoubak S, Rynditch A, Bernardi G. Compositional bimodality and evolution of retroviral genomes. Gene. 1992;119(2):207-13.
[104] Boiocchi M, Dolcetti R, Maestro R, Feriotto G, Rizzo S, De Re V, Sonego F. A coordinated proto-oncogene expression characterizes MCF 247 murine leukemia virus-induced T-cell lymphomas irrespectively of proviral insertion affecting myc loci. Leuk Res. 1990;14(6):549-58.
[105] Kratochwil K, von der Mark K, Kollar EJ, Jaenisch R, Mooslehner K, Schwarz M, Haase K, Gmachl I, Harbers K. Retrovirus-induced insertional mutation in Mov13 mice affects collagen I expression in a tissue-specific manner. Cell. 1989;57(5):807-16.
[106] Selten G, Cuypers HT, Berns A. Proviral activation of the putative oncogene Pim-1 in MuLV induced T-cell lymphomas. EMBO J. 1985;4(7):1793-8.
[107] Moreau-Gachelin F, Ray D, de Both NJ, van der Feltz MJ, Tambourin P, Tavitian A. Spi-1 oncogene activation in Rauscher and Friend murine virus-induced acute erythroleukemias. Leukemia. 1990;4(1):20-3.
[108] Soriano P, Meunier-Rotival M, Bernardi G. The distribution of interspersed repeats is nonuniform and conserved in the mouse and human genomes. Proc Natl Acad Sci U S A. 1983;80(7):1816-20.
[109] Flubacher MM, Bear SE, Tsichlis PN. Replacement of interleukin-2 (IL-2)-generated mitogenic signals by a mink cell focus-forming (MCF) or xenotropic virus-induced IL-9-dependent autocrine loop: implications for MCF virus-induced leukemogenesis. J Virol. 1994;68(12):7709-16.
[110] O'Donnell PV, Fleissner E, Lonial H, Koehne CF, Reicin A. Early clonality and high-frequency proviral integration into the c-myc locus in AKR leukemias. J Virol. 1985;55(2):500-3.
[111] van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A. Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell. 1991;65(5):737-52.
[112] Tremblay PJ, Kozak CA, Jolicoeur P. Identification of a novel gene, Vin-1, in murine leukemia virus-induced T-cell leukemias by provirus insertional mutagenesis. J Virol. 1992;66(3):1344-53.
[113] Wolf D, Admon S, Oren M, Rotter V. Abelson murine leukemia virus-transformed cells that lack p53 protein synthesis express aberrant p53 mRNA species. Mol Cell Biol. 1984;4(3):552-8.
[114] Voronova AF, Sefton BM. Expression of a new tyrosine protein kinase is stimulated by retrovirus promoter insertion. Nature. 1986 Feb 20-26;319(6055):682-5.
[115] Vijaya S, Steffen DL, Kozak C, Robinson HL. Dsi-1, a region with frequent proviral insertions in Moloney murine leukemia virus-induced rat thymomas. J Virol. 1987;61(4):1164-70.
[116] Gisselbrecht S, Fichelson S, Sola B, Bordereaux D, Hampe A, Andr? C, Galibert F, Tambourin P. Frequent c-fms activation by proviral insertion in mouse myeloblastic leukaemias. Nature. 1987 Sep 17-23;329(6136):259-61.
[117] Ihle JN, Smith-White B, Sisson B, Parker D, Blair DG, Schultz A, Kozak C, Lunsford RD, Askew D, Weinstein Y, et al. Activation of the c-H-ras proto-oncogene by retrovirus insertion and chromosomal rearrangement in a Moloney leukemia virus-induced T-cell leukemia. J Virol. 1989;63(7):2959-66.
[118] Ben-David Y, Giddens EB, Letwin K, Bernstein A. Erythroleukemia induction by Friend murine leukemia virus: insertional activation of a new member of the ets gene family, Fli-1, closely linked to c-ets-1. Genes Dev. 1991;5(6):908-18.
[119] Bear SE, Bellacosa A, Lazo PA, Jenkins NA, Copeland NG, Hanson C, Levan G, Tsichlis PN. Provirus insertion in Tpl-1, an Ets-1-related oncogene, is associated with tumor progression in Moloney murine leukemia virus-induced rat thymic lymphomas. Proc Natl Acad Sci U S A. 1989;86(19):7495-9.
[120] Makris A, Patriotis C, Bear SE, Tsichlis PN. Genomic organization and expression of Tpl-2 in normal cells and Moloney murine leukemia virus-induced rat T-cell lymphomas: activation by provirus insertion. J Virol. 1993;67(7):4283-9.
[121] Shimada Y, Migliaccio G, Ruscetti S, Adamson JW, Migliaccio AR. Expression of the interleukin-3 and granulocyte-macrophage colony-stimulating factor genes in Friend spleen focus-forming virus-induced erythroleukemia. Blood. 1992;79(9):2423-31.
[122] Ben-David Y, Bani MR, Chabot B, De Koven A, Bernstein A. Retroviral insertions downstream of the heterogeneous nuclear ribonucleoprotein A1 gene in erythroleukemia cells: evidence that A1 is not essential for cell growth. Mol Cell Biol. 1992;12(10):4449-55.
[123] Lu SJ, Rowan S, Bani MR, 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. 1994;91(18):8398-402.
[124] Matthews EA, Vasmel WL, Schoenmakers HJ, Melief CJ. Retrovirally induced murine B-cell tumors rarely show proviral integration in sites common in T-cell tumors. Int J Cancer. 1989;43(6):1120-5.
[125] Morishita K, Parker DS, Mucenski ML, Jenkins NA, Copeland NG, Ihle JN. Retroviral activation of a novel gene encoding a zinc finger protein in IL-3-dependent myeloid leukemia cell lines. Cell. 1988;54(6):831-40.
[126] George DL, Glick B, Trusko S, Freeman N. Enhanced c-Ki-ras expression associated with Friend virus integration in a bone marrow-derived mouse cell line. Proc Natl Acad Sci U S A. 1986;83(6):1651-5.
[127] Noori-Daloii MR, Swift RA, Kung HJ, Crittenden LB, Witter RL. Specific integration of REV proviruses in avian bursal lymphomas. Nature. 1981;294(5841):574-6.
[128] Kanter MR, Smith RE, Hayward WS. Rapid induction of B-cell lymphomas: insertional activation of c-myb by avian leukosis virus. J Virol. 1988;62(4):1423-32.
[129] Westaway D, Papkoff J, Moscovici C, Varmus HE. Identification of a provirally activated c-Ha-ras oncogene in an avian nephroblastoma via a novel procedure: cDNA cloning of a chimaeric viral-host transcript. EMBO J. 1986;5(2):301-9.
[130] Dickson C, Smith R, Brookes S, Peters G. Tumorigenesis by mouse mammary tumor virus: proviral activation of a cellular gene in the common integration region int-2. Cell. 1984;37(2):529-36.
[131] Chalker DL, Sandmeyer SB. Ty3 integrates within the region of RNA polymerase III transcription initiation. Genes Dev. 1992;6(1):117-28.
[132] Gilks CB, Bear SE, Grimes HL, Tsichlis PN. Progression of interleukin-2 (IL-2)-dependent rat T cell lymphoma lines to IL-2-independent growth following activation of a gene (Gfi-1) encoding a novel zinc finger protein. Mol Cell Biol. 1993;13(3):1759-68.
[133] Marchetti A, Buttitta F, Miyazaki S, Gallahan D, Smith GH, Callahan R. Int-6, a highly conserved, widely expressed gene, is mutated by mouse mammary tumor virus in mammary preneoplasia. J Virol. 1995;69(3):1932-8.