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Impact of HTLV-I Tax on cell cycle progression and the cellular DNA damage repair response

Oncogene volume 24, pages 5986–5995 (2005)Cite this article

Abstract

Human T-cell lymphotropic virus type I (HTLV-I) is the etiologic agent of adult T-cell leukemia (ATL), a rapidly progressing, clonal malignancy of CD4+ T lymphocytes. Fewer than one in 20 infected individuals typically develop ATL and the onset of this cancer occurs after decades of relatively symptom-free infection. Leukemic cells from ATL patients display extensive and varied forms of chromosomal abnormalities and this genomic instability is thought to be a major contributor to the development of ATL. HTLV-I encodes a regulatory protein, Tax, which is necessary and sufficient to transform cells and is therefore considered to be the viral oncoprotein. Tax interacts with numerous cellular proteins to reprogram cellular processes including, but not limited to, transcription, cell cycle regulation, DNA repair, and apoptosis. This review presents an overview of the impact of HTLV-I infection in general, and Tax expression in particular, on cell cycle progression and the repair of DNA damage. The contribution of these activities to genome instability and cellular transformation will be discussed.

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References

  • Abrieu A, Magnaghi-Jaulin L, Kahana JA, Peter M, Castro A, Vigneron S, Lorca T, Cleveland DW and Labbe JC . (2001). Cell, 106, 83–93.

  • Akagi T, Ono H and Shimotohno K . (1996). Oncogene, 12, 1645–1652.

  • Arlett CF, Ashby J, Fielder RJ and Scott D . (1989). Mutagenesis, 4, 482–485.

  • Ball KL . (1997). Prog. Cell Cycle Res., 3, 125–134.

  • Benhamou S and Sarasin A . (2000). Mutat. Res., 462, 149–158.

  • Cahill DP, Lengauer C, Yu J, Riggins GJ, Willson JK, Markowitz SD, Kinzler KW and Vogelstein B . (1998). Nature, 392, 300–303.

  • Castro A, Bernis C, Vigneron S, Labbe JC and Lorca T . (2005). Oncogene, 24, 314–325.

  • Cereseto A, Diella F, Mulloy JC, Cara A, Michieli P, Grassmann R, Franchini G and Klotman ME . (1996). Blood, 88, 1551–1560.

  • Chan GK and Yen TJ . (2003). Prog. Cell Cycle Res., 5, 431–439.

  • Chen RH, Brady DM, Smith D, Murray AW and Hardwick KG . (1999). Mol. Biol. Cell, 10, 2607–2618.

  • Chen Y and Sanchez Y . (2004). DNA Repair (Amsterdam), 3, 1025–1032.

  • Chieco-Bianchi L, Saggioro D, Del Mistro A, Montaldo A, Majone F and Levis AG . (1988). Leukemia, 2 (12 Suppl), 223S–232S.

  • De La Fuente C, Santiago F, Chong S, Deng L, Mayhood T, Fu P, Stein D, Denny T, Coffman F, Azimi N, Mahieux R and Kashanchi F . (2000). J. Virol., 74, 7270–7283.

  • Elder RT, Benko Z and Zhao Y . (2002). Front. Biosci., 7, d349–d357.

  • Franzese O, Balestrieri E, Comandini A, Forte G, Macchi B and Bonmassar E . (2002). AIDS Res. Hum. Retroviruses, 18, 249–251.

  • Fujimoto T, Hata T, Itoyama T, Nakamura H, Tsukasaki K, Yamada Y, Ikeda S, Sadamori N and Tomonaga M . (1999). Cancer Genet. Cytogenet., 109, 1–13.

  • Gabet AS, Mortreux F, Charneau P, Riou P, Duc-Dodon M, Wu Y, Jeang KT and Wattel E . (2003). Oncogene, 22, 3734–3741.

  • Gatza ML, Watt JC and Marriott SJ . (2003). Oncogene, 22, 5141–5149.

  • Haller K, Wu Y, Derow E, Schmitt I, Jeang KT and Grassmann R . (2002). Mol. Cell. Biol., 22, 3327–3338.

  • Hanawalt PC . (1986). Basic Life Sci., 38, 489–498.

  • Haoudi A, Daniels RC, Wong E, Kupfer G and Semmes OJ . (2003). J. Biol. Chem., 278, 37736–37744.

  • Haoudi A and Semmes OJ . (2003). Virology, 305, 229–239.

  • Harper JV and Brooks G . (2005). Methods Mol. Biol., 296, 113–153.

  • Hatta Y and Koeffler HP . (2002). Leukemia, 16, 1069–1085.

  • Hatta Y, Spirin K, Tasaka T, Morosetti R, Said JW, Yamada Y, Tomonaga M and Koeffler HP . (1997a). Br. J. Haematol., 99, 665–667.

  • Hatta Y, Yamada Y, Tomonaga M and Koeffler HP . (1997b). Leukemia, 11, 984–989.

  • Hatta Y, Yamada Y, Tomonaga M, Miyoshi I, Said JW and Koeffler HP . (1998). Br. J. Haematol., 101, 341–344.

  • Hayami Y, Komatsu H, Iida S, Utsunomiya A, Hanada S, Hua XJ, Huiping N, Harada S, Tsuboi K, Banno S, Wakita A, Kato T and Ueda R . (1999). Leuk. Lymphoma, 32, 345–349.

  • Herdegen T and Leah JD . (1998). Brain Res. Rev., 28, 370–490.

  • Hoeijmakers JH . (1993). Trends Genet., 9, 211–217.

  • Hoyt MA, Totis L and Roberts BT . (1991). Cell, 66, 507–517.

  • Huang Y, Ohtani K, Iwanaga R, Matsumura Y and Nakamura M . (2001). Oncogene, 20, 1094–1102.

  • Itoyama T, Sadamori N, Tokunaga S, Sasagawa I, Nakamura H, Yao E, Jubashi T, Yamada Y, Ikeda S and Ichimaru M . (1990). Cancer Genet. Cytogenet., 49, 157–163.

  • Iwanaga R, Ohtani K, Hayashi T and Nakamura M . (2001). Oncogene, 20, 2055–2067.

  • Jeang KT, Giam CZ, Majone F and Aboud M . (2004). J. Biol. Chem., 279, 31991–31994.

  • Jeang KT, Widen SG, Semmes OJt and Wilson SH . (1990). Science, 247, 1082–1084.

  • Jeong SJ, Radonovich M, Brady J and Pise-Masison CA . (2004). Blood, 104, 1490–1497.

  • Jin DY, Spencer F and Jeang KT . (1998). Cell, 93, 81–91.

  • Kamada Y, Iwamasa T, Miyazato M, Sunagawa K and Kunishima N . (1992). Cancer, 70, 861–868.

  • Kao SY, Lemoine FJ and Marriott SJ . (2000). J. Biol. Chem., 275, 35926–35931.

  • Kao SY and Marriott SJ . (1999). J. Virol., 73, 4299–4304.

  • Kasai T, Iwanaga Y, Iha H and Jeang KT . (2002). J. Biol. Chem., 277, 5187–5193.

  • Kawata S, Ariumi Y and Shimotohno K . (2003). J. Virol., 77, 7291–7299.

  • Kehn K, Deng L, De La Fuente C, Strouss K, Wu K, Maddukuri A, Baylor S, Rufner R, Pumfery A, Bottazzi ME and Kashanchi F . (2004). Retrovirology, 1, 6.

  • Kehn K, Fuente Cde L, Strouss K, Berro R, Jiang H, Brady J, Mahieux R, Pumfery A, Bottazzi ME and Kashanchi F . (2005). Oncogene, 24, 525–540.

  • Kelman Z . (1997). Oncogene, 14, 629–640.

  • Kibler KV and Jeang KT . (2001). J. Virol., 75, 2161–2173.

  • Kino T and Pavlakis GN . (2004). DNA Cell Biol., 23, 193–205.

  • Kinoshita T, Imamura J, Nagai H and Shimotohno K . (1992). Anal. Biochem., 206, 231–235.

  • LaBaer J, Garrett MD, Stevenson LF, Slingerland JM, Sandhu C, Chou HS, Fattaey A and Harlow E . (1997). Genes Dev., 8, 1750–1758.

  • Lemasson I, Thebault S, Sardet C, Devaux C and Mesnard JM . (1998). J. Biol. Chem., 273, 23598–23604.

  • Lemoine FJ, Kao SY and Marriott SJ . (2000). AIDS Res. Hum. Retroviruses, 16, 1623–1627.

  • Lemoine FJ and Marriott SJ . (2001). J. Biol. Chem., 276, 31851–31857.

  • Lemoine FJ and Marriott SJ . (2002). Oncogene, 21, 7230–7234.

  • Lemoine FJ, Wycuff DR and Marriott SJ . (2001). Dis. Markers, 17, 129–137.

  • Li R and Murray AW . (1991). Cell, 66, 519–531.

  • Liang MH, Geisbert T, Yao Y, Hinrichs SH and Giam CZ . (2002). J. Virol., 76, 4022–4033.

  • Liu B, Hong S, Tang Z, Yu H and Giam CZ . (2005). Proc. Natl. Acad. Sci. USA, 102, 63–68.

  • Liu B, Liang MH, Kuo YL, Liao W, Boros I, Kleinberger T, Blancato J and Giam CZ . (2003). Mol. Cell. Biol., 23, 5269–5281.

  • Low KG, Dorner LF, Fernando DB, Grossman J, Jeang KT and Comb MJ . (1997). J. Virol., 71, 1956–1962.

  • Majone F and Jeang KT . (2000). J. Biol. Chem., 275, 32906–32910.

  • Majone F, Semmes OJ and Jeang KT . (1993). Virology, 193, 456–459.

  • Maruyama K, Fukushima T, Kawamura K and Mochizuki S . (1990). Cancer Res., 50 (17 Suppl), 5697S–5702S.

  • Miyake H, Suzuki T, Hirai H and Yoshida M . (1999). Virology, 253, 155–161.

  • Morimoto H, Tsukada J, Kominato Y and Tanaka Y . (2005). Am. J. Hematol., 78, 100–107.

  • Mozzherin DJ, McConnell M, Jasko MV, Krayevsky AA, Tan CK, Downey KM and Fisher PA . (1996). J. Biol. Chem., 271, 31711–31717.

  • Mozzherin DJ, Shibutani S, Tan CK, Downey KM and Fisher PA . (1997). Proc. Natl. Acad. Sci. USA, 94, 6126–6131.

  • Mulloy JC, Kislyakova T, Cereseto A, Casareto L, LoMonico A, Fullen J, Lorenzi MV, Cara A, Nicot C, Giam C and Franchini G . (1998). J. Virol., 72, 8852–8860.

  • Murphy EL, Hanchard B, Figueroa JP, Gibbs WN, Lofters WS, Campbell M, Goedert JJ and Blattner WA . (1989). Int. J. Cancer, 43, 250–253.

  • Musacchio A and Hardwick KG . (2002). Nat. Rev. Mol. Cell. Biol., 3, 731–741.

  • Nerenberg M, Hinrichs SH, Reynolds RK, Khoury G and Jay G . (1987). Science, 237, 1324–1329.

  • Neuveut C and Jeang KT . (2000). Prog. Cell Cycle Res., 4, 157–162.

  • Ng PW, Iha H, Iwanaga Y, Bittner M, Chen Y, Jiang Y, Gooden G, Trent JM, Meltzer P, Jeang KT and Zeichner SL . (2001). Oncogene, 20, 4484–4496.

  • Nowell PC . (1976). Science, 194, 23–28.

  • Ohshima K, Haraoka S, Yoshioka S, Hamasaki M, Fujiki T, Suzumiya J, Kawasaki C, Kanda M and Kikuchi M . (2000). Cancer Lett., 158, 141–150.

  • Ohshima K, Ohgami A, Matsuoka M, Etoh K, Utsunomiya A, Makino T, Ishiguro M, Suzumiya J and Kikuchi M . (1998). Cancer Lett., 132, 203–212.

  • Ohtani K, Iwanaga R, Arai M, Huang Y, Matsumura Y and Nakamura M . (2000). J. Biol. Chem., 275, 11154–11163.

  • Okamoto T, Ohno Y, Tsugane S, Watanabe S, Shimoyama M, Tajima K, Miwa M and Shimotohno K . (1989). Jpn. J. Cancer Res., 80, 191–195.

  • Park HU, Jeong JH, Chung JH and Brady JN . (2004). Oncogene, 23, 4966–4974.

  • Parry JM and Parry EM . (1987). Mutat. Res., 181, 267–287.

  • Philpott SM and Buehring GC . (1999). J. Natl. Cancer Inst., 91, 933–942.

  • Pise-Masison CA, Choi KS, Radonovich M, Dittmer J, Kim SJ and Brady J . (1998). J. Virol., 72, 1165–1170.

  • Pise-Masison CA, Mahieux R, Jiang H, Ashcroft M, Radonovich M, Duvall J, Guillerm C and Brady J . (2000). Mol. Cell. Biol., 20, 3377–3386.

  • Ressler S, Morris GF and Marriott SJ . (1997). J. Virol., 71, 1181–1190.

  • Sadamori N . (1991). Cancer Genet. Cytogenet., 51, 131–136.

  • Saggioro D, Majone F, Forino M, Turchetto L, Leszl A and Chieco-Bianchi L . (1994). Leuk. Lymphoma, 12, 281–286.

  • Sakashita A, Hattori T, Miller CW, Suzushima H, Asou N, Takatsuki K and Koeffler HP . (1992). Blood, 79, 477–480.

  • Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K and Linn S . (2004). Annu. Rev. Biochem., 73, 39–85.

  • Sandberg AA . (1980). Cancer, 46, 2221–2226.

  • Santiago F, Clark E, Chong S, Molina C, Mozafari F, Mahieux R, Fujii M, Azimi N and Kashanchi F . (1999). J. Virol., 73, 9917–9927.

  • Seiki M, Eddy R, Shows TB and Yoshida M . (1984). Nature, 309, 640–642.

  • Semmes OJ, Majone F, Cantemir C, Turchetto L, Hjelle B and Jeang KT . (1996). Virology, 217, 373–379.

  • Sherr CJ and Roberts JM . (1999). Genes Dev., 13, 1501–1512.

  • Shimoyama M . (1991). Br. J. Haematol., 79, 428–437.

  • Sinha-Datta U, Horikawa I, Michishita E, Datta A, Sigler-Nicot JC, Brown M, Kazanji M, Barrett JC and Nicot C . (2004). Blood, 104, 2523–2531.

  • Smith MR and Greene WC . (1991). J. Clin. Invest., 87, 761–766.

  • Suzuki T, Narita T, Uchida-Toita M and Yoshida M . (1999a). Virology, 259, 384–391.

  • Suzuki T, Uchida-Toita M and Yoshida M . (1999b). Oncogene, 18, 4137–4143.

  • Tanaka A, Takahashi C, Yamaoka S, Nosaka T, Maki M and Hatanaka M . (1990). Proc. Natl. Acad. Sci. USA, 87, 1071–1075.

  • Thomson EJ and Perry PE . (1988). Mutagenesis, 3, 415–418.

  • Tighe A, Johnson VL, Albertella M and Taylor SS . (2001). EMBO Rep., 2, 609–614.

  • Tsumuki H, Nakazawa M, Hasunuma T, Kobata T, Kato T, Uchida A and Nishioka K . (2001). Rheumatol. Int., 20, 175–179.

  • Tyler KL, Clarke P, DeBiasi RL, Kominsky D and Poggioli GJ . (2001). Trends Microbiol., 9, 560–564.

  • Uchida N, Otsuka T, Arima F, Shigematsu H, Fukuyama T, Maeda M, Sugio Y, Itoh Y and Niho Y . (1999). Leuk. Res., 23, 311–316.

  • Van Orden K and Nyborg JK . (2000). Gene Expression, 9, 29–36.

  • Van PL, Yim KW, Jin DY, Diapolito G, Kurimasa A and Jeang KT . (2001). J. Virol., 75, 396–407.

  • Walker DH and Maller JL . (1991). Nature, 354, 314–317.

  • Wasch R and Engelbert D . (2005). Oncogene, 24, 1–10.

  • Whang-Peng J, Bunn PA, Knutsen T, Kao-Shan CS, Broder S, Jaffe ES, Gelmann E, Blattner W, Lofters W, Young RC and Gallo RC . (1985). J. Natl. Cancer Inst., 74, 357–369.

  • Wilson S, Abbotts J and Widen S . (1988). Biochim. Biophys. Acta, 949, 149–157.

  • Wood RD and Shivji MK . (1997). Carcinogenesis, 18, 605–610.

  • Yamaoka S, Tobe T and Hatanaka M . (1992). Oncogene, 7, 433–437.

  • Yamato K, Oka T, Hiroi M, Iwahara Y, Sugito S, Tsuchida N and Miyoshi I . (1993). Jpn. J. Cancer Res., 84, 4–8.

  • Yoshida M . (2001). Annu. Rev. Immunol., 19, 475–496.

  • Zhou BB and Elledge SJ . (2000). Nature, 408, 433–439.

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Acknowledgements

We are grateful to members of the HTLV research community for years of fruitful collaboration and discussion in a collegial scientific environment. We would also like to thank members of the Marriott and Semmes laboratories for helpful suggestions and editorial comments. The Marriott Lab is supported by Public Health Service Grants CA-77371 and CA-55684 awarded to SJM from the National Cancer Institute. The Semmes Lab is supported by Public Health Service Grants CA-76595 and CA-85067 awarded to OJS from the National Cancer Institute.

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  1. Department of Molecular Virology and Microbiology, Baylor College of Medicine, One Baylor Plaza, Houston, 77030, TX, USA

    Susan J Marriott

  2. Department of Microbiology and Molecular Cell Biology, Eastern Virginia Medical School, Norfolk, 23508, VA, USA

    Oliver John Semmes

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Marriott, S., Semmes, O. Impact of HTLV-I Tax on cell cycle progression and the cellular DNA damage repair response. Oncogene 24, 5986–5995 (2005). https://doi.org/10.1038/sj.onc.1208976

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