The role of HBZ in HTLV-1-induced oncogenesis

Viruses

Volumn 8, Issue 2, 2016, Pages

  Zhao, Tiejun ^a  

^a ZHEJIANG NORMAL UNIVERSITY   (China)

Author keywords

ATL; HBZ; HTLV 1

Indexed keywords

APOPTOSIS; CARCINOGENESIS; CELL PROLIFERATION; CELLULAR IMMUNITY; GENE EXPRESSION; HUMAN T-LYMPHOTROPIC VIRUS 1; INFLAMMATION; NONHUMAN; OPEN READING FRAME; REVIEW; VIRUS REPLICATION; ANIMAL; CELL TRANSFORMATION; GENETICS; HUMAN; METABOLISM; T CELL LEUKEMIA; VIROLOGY;

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; HBZ PROTEIN, HUMAN T-CELL LEUKEMIA VIRUS TYPE I; VIRAL PROTEIN;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CARCINOGENESIS; CELL TRANSFORMATION, NEOPLASTIC; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; LEUKEMIA-LYMPHOMA, ADULT T-CELL; RETROVIRIDAE PROTEINS;

EID: 84957546900     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v8020034     Document Type: Review

References (90)

1. Uchiyama, T.; Yodoi, J.; Sagawa, K.; Takatsuki, K.; Uchino, H. Adult T-cell leukemia: Clinical and hematologic features of 16 cases. Blood 1977, 50, 481-492. [CrossRef].
2. Poiesz, B.J.; Ruscetti, F.W.; Gazdar, A.F.; Bunn, P.A.; Minna, J.D.; Gallo, R.C. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc. Natl. Acad. Sci. USA 1980, 77, 7415-7419. [CrossRef] [PubMed].
3. Gessain, A.; Barin, F.; Vernant, J.C.; Gout, O.; Maurs, L.; Calender, A.; de The, G. Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet 1985, 2, 407-410. [CrossRef].
4. Osame, M.; Usuku, K.; Izumo, S.; Ijichi, N.; Amitani, H.; Igata, A.; Matsumoto, M.; Tara, M. HTLV-I associated myelopathy, a new clinical entity. Lancet 1986, 1, 1031-1032. [CrossRef].
5. Matsuoka, M.; Jeang, K.T. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat. Rev. Cancer 2007, 7, 270-280. [CrossRef] [PubMed].
6. Gaudray, G.; Gachon, F.; Basbous, J.; Biard-Piechaczyk, M.; Devaux, C.; Mesnard, J.M. The complementary strand of the human T-cell leukemia virus type 1 RNA genome encodes a bZIP transcription factor that down-regulates viral transcription. J. Virol. 2002, 76, 12813-12822. [CrossRef] [PubMed].
7. Nicot, C.; Harrod, R.L.; Ciminale, V.; Franchini, G. Human T-cell leukemia/lymphoma virus type 1 nonstructural genes and their functions. Oncogene 2005, 24, 6026-6034. [CrossRef] [PubMed].
8. Grassmann, R.; Aboud, M.; Jeang, K.T. Molecular mechanisms of cellular transformation by HTLV-1 Tax. Oncogene 2005, 24, 5976-5985. [CrossRef] [PubMed].
9. Giam, C.Z.; Jeang, K.T. HTLV-1 Tax and adult T-cell leukemia. Front. Biosci. 2007, 12, 1496-1507. [CrossRef] [PubMed].
10. Yoshida, M. HTLV-1 Tax: Regulation of gene expression and disease. Trends Microbiol. 1993, 1, 131-135. [CrossRef].
11. Takeda, S.; Maeda, M.; Morikawa, S.; Taniguchi, Y.; Yasunaga, J.; Nosaka, K.; Tanaka, Y.; Matsuoka, M. Genetic and epigenetic inactivation of tax gene in adult T-cell leukemia cells. Int. J. Cancer 2004, 109, 559-567. [CrossRef].
12. Satou, Y.; Yasunaga, J.; Yoshida, M.; Matsuoka, M. HTLV-I basic leucine zipper factor gene mRNA supports proliferation of adult T cell leukemia cells. Proc. Natl. Acad. Sci. USA 2006, 103, 720-725. [CrossRef].
13. Fan, J.; Ma, G.; Nosaka, K.; Tanabe, J.; Satou, Y.; Koito, A.; Wain-Hobson, S.; Vartanian, J.P.; Matsuoka, M. APOBEC3G generates nonsense mutations in human T-cell leukemia virus type 1 proviral genomes in vivo. J. Virol. 2010, 84, 7278-7287. [CrossRef] [PubMed].
14. Kannagi, M.; Harada, S.; Maruyama, I.; Inoko, H.; Igarashi, H.; Kuwashima, G.; Sato, S.; Morita, M.; Kidokoro, M.; Sugimoto, M. et al. Predominant recognition of human T cell leukemia virus type I (HTLV-I) pX gene products by human CD8+ cytotoxic T cells directed against HTLV-I-infected cells. Int. Immunol. 1991, 3, 761-767. [CrossRef].
15. Suemori, K.; Fujiwara, H.; Ochi, T.; Ogawa, T.; Matsuoka, M.; Matsumoto, T.; Mesnard, J.M.; Yasukawa, M. HBZ is an immunogenic protein, but not a target antigen for human T-cell leukemia virus type 1-specific cytotoxic T lymphocytes. J. Gen. Virol. 2009, 90, 1806-1811. [CrossRef] [PubMed].
16. Rowan, A.G.; Suemori, K.; Fujiwara, H.; Yasukawa, M.; Tanaka, Y.; Taylor, G.P.; Bangham, C.R. Cytotoxic T lymphocyte lysis of HTLV-1 infected cells is limited by weak HBZ protein expression, but non-specifically enhanced on induction of Tax expression. Retrovirology 2014, 11. [CrossRef].
17. Sugata, K.; Yasunaga, J.; Mitobe, Y.; Miura, M.; Miyazato, P.; Kohara, M.; Matsuoka, M. Protective effect of cytotoxic T lymphocytes targeting HTLV-1 bZIP factor. Blood 2015, 126, 1095-1105. [CrossRef] [PubMed].
18. Matsuoka, M.; Green, P.L. The HBZ gene, a key player in HTLV-1 pathogenesis. Retrovirology 2009, 6. [CrossRef] [PubMed].
19. Zhao, T.; Matsuoka, M. HBZ and its roles in HTLV-1 oncogenesis. Front. Microbiol. 2012, 3. [CrossRef] [PubMed].
20. Yamaoka, S.; Tobe, T.; Hatanaka, M. Tax protein of human T-cell leukemia virus type I is required for maintenance of the transformed phenotype. Oncogene 1992, 7, 433-437. [PubMed].
21. Tamiya, S.; Matsuoka, M.; Etoh, K.; Watanabe, T.; Kamihira, S.; Yamaguchi, K.; Takatsuki, K. Two types of defective human T-lymphotropic virus type I provirus in adult T-cell leukemia. Blood 1996, 88, 3065-3073. [PubMed].
22. Miyazaki, M.; Yasunaga, J.; Taniguchi, Y.; Tamiya, S.; Nakahata, T.; Matsuoka, M. Preferential selection of human T-cell leukemia virus type 1 provirus lacking the 5' long terminal repeat during oncogenesis. J. Virol. 2007, 81, 5714-5723. [CrossRef] [PubMed].
23. Furukawa, Y.; Kubota, R.; Tara, M.; Izumo, S.; Osame, M. Existence of escape mutant in HTLV-I tax during the development of adult T-cell leukemia. Blood 2001, 97, 987-993. [CrossRef].
24. Koiwa, T.; Hamano-Usami, A.; Ishida, T.; Okayama, A.; Yamaguchi, K.; Kamihira, S.; Watanabe, T. 5'-long terminal repeat-selective CpG methylation of latent human T-cell leukemia virus type 1 provirus in vitro and in vivo. J. Virol. 2002, 76, 9389-9397. [CrossRef] [PubMed].
25. Taniguchi, Y.; Nosaka, K.; Yasunaga, J.; Maeda, M.; Mueller, N.; Okayama, A.; Matsuoka, M. Silencing of human T-cell leukemia virus type I gene transcription by epigenetic mechanisms. Retrovirology 2005, 2. [CrossRef] [PubMed].
26. Yoshida, M.; Satou, Y.; Yasunaga, J.; Fujisawa, J.; Matsuoka, M. Transcriptional control of spliced and unspliced human T-cell leukemia virus type 1 bZIP factor (HBZ) gene. J. Virol. 2008, 82, 9359-9368. [CrossRef] [PubMed].
27. Saito, M.; Matsuzaki, T.; Satou, Y.; Yasunaga, J.; Saito, K.; Arimura, K.; Matsuoka, M.; Ohara, Y. In vivo expression of the HBZ gene of HTLV-1 correlates with proviral load, inflammatory markers and disease severity in HTLV-1 associated myelopathy/tropical spastic paraparesis (HAM/TSP). Retrovirology 2009, 6. [CrossRef] [PubMed].
28. Usui, T.; Yanagihara, K.; Tsukasaki, K.; Murata, K.; Hasegawa, H.; Yamada, Y.; Kamihira, S. Characteristic expression of HTLV-1 basic zipper factor (HBZ) transcripts in HTLV-1 provirus-positive cells. Retrovirology 2008, 5. [CrossRef] [PubMed].
29. Li, M.; Kesic, M.; Yin, H.; Yu, L.; Green, P.L. Kinetic analysis of human T-cell leukemia virus type 1 gene expression in cell culture and infected animals. J. Virol. 2009, 83, 3788-3797. [CrossRef].
30. Cavanagh, M.H.; Landry, S.; Audet, B.; Arpin-Andre, C.; Hivin, P.; Pare, M.E.; Thete, J.; Wattel, E.; Marriott, S.J.; Mesnard, J.M.; Barbeau, B. HTLV-I antisense transcripts initiating in the 3'LTR are alternatively spliced and polyadenylated. Retrovirology 2006, 3. [CrossRef] [PubMed].
31. Murata, K.; Hayashibara, T.; Sugahara, K.; Uemura, A.; Yamaguchi, T.; Harasawa, H.; Hasegawa, H.; Tsuruda, K.; Okazaki, T.; Koji, T. et al. A novel alternative splicing isoform of human T-cell leukemia virus type 1 bZIP factor (HBZ-SI) targets distinct subnuclear localization. J. Virol. 2006, 80, 2495-2505. [CrossRef] [PubMed].
32. Arnold, J.; Zimmerman, B.; Li, M.; Lairmore, M.D.; Green, P.L. Human T-cell leukemia virus type-1 antisense-encoded gene, Hbz, promotes T-lymphocyte proliferation. Blood 2008, 112, 3788-3797. [CrossRef] [PubMed].
33. Raval, G.U.; Bidoia, C.; Forlani, G.; Tosi, G.; Gessain, A.; Accolla, R.S. Localization, quantification and interaction with host factors of endogenous HTLV-1 HBZ protein in infected cells and ATL. Retrovirology 2015, 12. [CrossRef] [PubMed].
34. Boam, D.S.; Davidson, I.; Chambon, P. A TATA-less promoter containing binding sites for ubiquitous transcription factors mediates cell type-specific regulation of the gene for transcription enhancer factor-1 (TEF-1). J. Biol. Chem. 1995, 270, 19487-19494.
35. Liu, S.; Cowell, J.K. Cloning and characterization of the TATA-less promoter from the human GFI1 proto-oncogene. Ann. Hum. Genet. 2000, 64, 83-86. [CrossRef] [PubMed].
36. Landry, S.; Halin, M.; Vargas, A.; Lemasson, I.; Mesnard, J.M.; Barbeau, B. Upregulation of human T-cell leukemia virus type 1 antisense transcription by the viral Tax protein. J. Virol. 2009, 83, 2048-2054. [CrossRef] [PubMed].
37. Hivin, P.; Frederic, M.; Arpin-Andre, C.; Basbous, J.; Gay, B.; Thebault, S.; Mesnard, J.M. Nuclear localization of HTLV-I bZIP factor (HBZ) is mediated by three distinct motifs. J. Cell Sci. 2005, 118, 1355-1362. [CrossRef] [PubMed].
38. Zhao, T.; Satou, Y.; Sugata, K.; Miyazato, P.; Green, P.L.; Imamura, T.; Matsuoka, M. HTLV-1 bZIP factor enhances TGF-beta signaling through p300 coactivator. Blood 2011, 118, 1865-1876. [CrossRef] [PubMed].
39. Mukai, R.; Ohshima, T. HTLV-1 HBZ positively regulates the mTOR signaling pathway via inhibition of GADD34 activity in the cytoplasm. Oncogene 2014, 33, 2317-2328. [CrossRef] [PubMed].
40. Dissinger, N.; Shkriabai, N.; Hess, S.; Al-Saleem, J.; Kvaratskhelia, M.; Green, P.L. Identification and characterization of HTLV-1 HBZ post-translational modifications. PLoS ONE 2014, 9, e112762.
41. Ma, Y.; Zheng, S.; Wang, Y.; Zang, W.; Li, M.; Wang, N.; Li, P.; Jin, J.; Dong, Z.; Zhao, G. The HTLV-1 HBZ protein inhibits cyclin D1 expression through interacting with the cellular transcription factor CREB. Mol. Biol. Rep. 2013, 40, 5967-5975. [CrossRef] [PubMed].
42. Clerc, I.; Polakowski, N.; Andre-Arpin, C.; Cook, P.; Barbeau, B.; Mesnard, J.M.; Lemasson, I. An interaction between the human T cell leukemia virus type 1 basic leucine zipper factor (HBZ) and the KIX domain of p300/CBP contributes to the down-regulation of Tax-dependent viral transcription by HBZ. J. Biol. Chem. 2008, 283, 23903-23913. [CrossRef] [PubMed].
43. Cook, P.R.; Polakowski, N.; Lemasson, I. HTLV-1 HBZ protein deregulates interactions between cellular factors and the KIX domain of p300/CBP. J. Mol. Biol. 2011, 409, 384-398. [CrossRef] [PubMed].
44. Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646-674. [CrossRef] [PubMed].
45. Hanahan, D.; Weinberg, R.A. The hallmarks of cancer. Cell 2000, 100, 57-70. [CrossRef].
46. Satou, Y.; Yasunaga, J.; Zhao, T.; Yoshida, M.; Miyazato, P.; Takai, K.; Shimizu, K.; Ohshima, K.; Green, P.L.; Ohkura, N. et al. HTLV-1 bZIP factor induces T-cell lymphoma and systemic inflammation in vivo. PLoS Pathog. 2011, 7, e1001274. [CrossRef] [PubMed].
47. Mitobe, Y.; Yasunaga, J.; Furuta, R.; Matsuoka, M. HTLV-1 bZIP factor RNA and protein impart distinct functions on T-cell proliferation and survival. Cancer Res. 2015, 75, 4143-4152. [CrossRef] [PubMed].
48. Zhao, T.; Coutts, A.; Xu, L.; Yu, J.; Ohshima, K.; Matsuoka, M. HTLV-1 bZIP factor supports proliferation of adult T cell leukemia cells through suppression of C/EBP signaling. Retrovirology 2013, 10. [CrossRef] [PubMed].
49. Hagiya, K.; Yasunaga, J.; Satou, Y.; Ohshima, K.; Matsuoka, M. ATF3, an HTLV-1 bZip factor binding protein, promotes proliferation of adult T-cell leukemia cells. Retrovirology 2011, 8. [CrossRef] [PubMed].
50. Esquela-Kerscher, A.; Slack, F.J. Oncomirs—microRNAs with a role in cancer. Nat. Rev. Cancer 2006, 6, 259-269. [CrossRef] [PubMed].
51. Vernin, C.; Thenoz, M.; Pinatel, C.; Gessain, A.; Gout, O.; Delfau-Larue, M.H.; Nazaret, N.; Legras-Lachuer, C.; Wattel, E.; Mortreux, F. HTLV-1 bZIP factor HBZ promotes cell proliferation and genetic instability by activating OncomiRs. Cancer Res. 2014, 74, 6082-6093. [CrossRef] [PubMed].
52. Polakowski, N.; Terol, M.; Hoang, K.; Nash, I.; Laverdure, S.; Gazon, H.; Belrose, G.; Mesnard, J.M.; Cesaire, R.; Peloponese, J.M. et al. HBZ stimulates brain-derived neurotrophic factor/TrkB autocrine/paracrine signaling to promote survival of human T-cell leukemia virus type 1-Infected T cells. J. Virol. 2014, 88, 13482-13494. [CrossRef] [PubMed].
53. Ma, G.; Yasunaga, J.; Fan, J.; Yanagawa, S.; Matsuoka, M. HTLV-1 bZIP factor dysregulates the Wnt pathways to support proliferation and migration of adult T-cell leukemia cells. Oncogene 2013, 32, 4222-4230. [CrossRef] [PubMed].
54. Basbous, J.; Arpin, C.; Gaudray, G.; Piechaczyk, M.; Devaux, C.; Mesnard, J.M. The HBZ factor of human T-cell leukemia virus type I dimerizes with transcription factors JunB and c-Jun and modulates their transcriptional activity. J. Biol. Chem. 2003, 278, 43620-43627. [CrossRef] [PubMed].
55. Hivin, P.; Basbous, J.; Raymond, F.; Henaff, D.; Arpin-Andre, C.; Robert-Hebmann, V.; Barbeau, B.; Mesnard, J.M. The HBZ-SP1 isoform of human T-cell leukemia virus type I represses JunB activity by sequestration into nuclear bodies. Retrovirology 2007, 4. [CrossRef] [PubMed].
56. Matsumoto, J.; Ohshima, T.; Isono, O.; Shimotohno, K. HTLV-1 HBZ suppresses AP-1 activity by impairing both the DNA-binding ability and the stability of c-Jun protein. Oncogene 2005, 24, 1001-1010. [CrossRef] [PubMed].
57. Thebault, S.; Basbous, J.; Hivin, P.; Devaux, C.; Mesnard, J.M. HBZ interacts with JunD and stimulates its transcriptional activity. FEBS Lett. 2004, 562, 165-170. [CrossRef].
58. Kuhlmann, A.S.; Villaudy, J.; Gazzolo, L.; Castellazzi, M.; Mesnard, J.M.; Duc Dodon, M. HTLV-1 HBZ cooperates with JunD to enhance transcription of the human telomerase reverse transcriptase gene (hTERT). Retrovirology 2007, 4. [CrossRef] [PubMed].
59. Borowiak, M.; Kuhlmann, A.S.; Girard, S.; Gazzolo, L.; Mesnard, J.M.; Jalinot, P.; Dodon, M.D. HTLV-1 bZIP factor impedes the menin tumor suppressor and upregulates JunD-mediated transcription of the hTERT gene. Carcinogenesis 2013, 34, 2664-2672. [CrossRef] [PubMed].
60. Saggioro, D.; Silic-Benussi, M.; Biasiotto, R.; D’Agostino, D.M.; Ciminale, V. Control of cell death pathways by HTLV-1 proteins. Front. Biosci. 2009, 14, 3338-3351. [CrossRef].
61. Tanaka-Nakanishi, A.; Yasunaga, J.; Takai, K.; Matsuoka, M. HTLV-1 bZIP factor suppresses apoptosis by attenuating the function of FoxO3a and altering its localization. Cancer Res. 2014, 74, 188-200. [CrossRef] [PubMed].
62. Yamaoka, S.; Inoue, H.; Sakurai, M.; Sugiyama, T.; Hazama, M.; Yamada, T.; Hatanaka, M. Constitutive activation of NF-_B is essential for transformation of rat fibroblasts by the human T-cell leukemia virus type I Tax protein. EMBO J. 1996, 15, 873-887. [PubMed].
63. Sun, S.C.; Yamaoka, S. Activation of NF-_B by HTLV-I and implications for cell transformation. Oncogene 2005, 24, 5952-5964. [CrossRef] [PubMed].
64. Zhi, H.; Yang, L.; Kuo, Y.L.; Ho, Y.K.; Shih, H.M.; Giam, C.Z. NF-B hyper-activation by HTLV-1 tax induces cellular senescence, but can be alleviated by the viral anti-sense protein HBZ. PLoS Pathog. 2011, 7, e1002025. [CrossRef] [PubMed].
65. Zhao, T.; Yasunaga, J.; Satou, Y.; Nakao, M.; Takahashi, M.; Fujii, M.; Matsuoka, M. Human T-cell leukemia virus type 1 bZIP factor selectively suppresses the classical pathway of NF-B. Blood 2009, 113, 2755-2764. [CrossRef] [PubMed].
66. Wurm, T.; Wright, D.G.; Polakowski, N.; Mesnard, J.M.; Lemasson, I. The HTLV-1-encoded protein HBZ directly inhibits the acetyl transferase activity of p300/CBP. Nucleic Acids Res. 2012, 40, 5910-5925. [CrossRef] [PubMed].
67. Philip, S.; Zahoor, M.A.; Zhi, H.; Ho, Y.K.; Giam, C.Z. Regulation of human T-lymphotropic virus type I latency and reactivation by HBZ and Rex. PLoS Pathog. 2014, 10, e1004040. [CrossRef] [PubMed].
68. Beinke, S.; Ley, S.C. Functions of NF-B1 and NF-B2 in immune cell biology. Biochem. J. 2004, 382, 393-409. [CrossRef].
69. Saitoh, Y.; Yamamoto, N.; Dewan, M.Z.; Sugimoto, H.; Martinez Bruyn, V.J.; Iwasaki, Y.; Matsubara, K.; Qi, X.; Saitoh, T.; Imoto, I. et al. Overexpressed NF-кB-inducing kinase contributes to the tumorigenesis of adult T-cell leukemia and Hodgkin Reed-Sternberg cells. Blood 2008, 111, 5118-5129. [CrossRef].
70. Karube, K.; Ohshima, K.; Tsuchiya, T.; Yamaguchi, T.; Kawano, R.; Suzumiya, J.; Utsunomiya, A.; Harada, M.; Kikuchi, M. Expression of FoxP3, a key molecule in CD4CD25 regulatory T cells, in adult T-cell leukaemia/lymphoma cells. Br. J. Haematol. 2004, 126, 81-84. [CrossRef] [PubMed].
71. Bommireddy, R.; Doetschman, T. TGF-, T-cell tolerance and anti-CD3 therapy. Trends Mol. Med. 2004, 10, 3-9. [CrossRef] [PubMed].
72. Niitsu, Y.; Urushizaki, Y.; Koshida, Y.; Terui, K.; Mahara, K.; Kohgo, Y.; Urushizaki, I. Expression of TGF- gene in adult T cell leukemia. Blood 1988, 71, 263-266. [PubMed].
73. Arnulf, B.; Villemain, A.; Nicot, C.; Mordelet, E.; Charneau, P.; Kersual, J.; Zermati, Y.; Mauviel, A.; Bazarbachi, A.; Hermine, O. Human T-cell lymphotropic virus oncoprotein Tax represses TGF-beta 1 signaling in human T cells via c-Jun activation: A potential mechanism of HTLV-I leukemogenesis. Blood 2002, 100, 4129-4138. [CrossRef].
74. Lee, D.K.; Kim, B.C.; Brady, J.N.; Jeang, K.T.; Kim, S.J. Human T-cell lymphotropic virus type 1 tax inhibits transforming growth factor-beta signaling by blocking the association of Smad proteins with Smad-binding element. J. Biol. Chem. 2002, 277, 33766-33775. [CrossRef] [PubMed].
75. Mori, N.; Morishita, M.; Tsukazaki, T.; Giam, C.Z.; Kumatori, A.; Tanaka, Y.; Yamamoto, N. Human T-cell leukemia virus type I oncoprotein Tax represses Smad-dependent transforming growth factor signaling through interaction with CREB-binding protein/p300. Blood 2001, 97, 2137-2144. [CrossRef] [PubMed].
76. Cheng, P.L.; Chang, M.H.; Chao, C.H.; Lee, Y.H. Hepatitis C viral proteins interact with Smad3 and differentially regulate TGF-/Smad3-mediated transcriptional activation. Oncogene 2004, 23, 7821-7838. [CrossRef].
77. Lee, D.K.; Park, S.H.; Yi, Y.; Choi, S.G.; Lee, C.; Parks, W.T.; Cho, H.; de Caestecker, M.P.; Shaul, Y.; Roberts, A.B.; Kim, S.J. The hepatitis B virus encoded oncoprotein pX amplifies TGF-β family signaling through direct interaction with Smad4: Potential mechanism of hepatitis B virus-induced liver fibrosis. Genes Dev. 2001, 15, 455-466. [CrossRef] [PubMed].
78. Prokova, V.; Mosialos, G.; Kardassis, D. Inhibition of transforming growth factor beta signaling and Smad-dependent activation of transcription by the Latent Membrane Protein 1 of Epstein-Barr virus. J. Biol. Chem. 2002, 277, 9342-9350. [CrossRef] PubMed].
79. Tomita, M.; Choe, J.; Tsukazaki, T.; Mori, N. The Kaposi’s sarcoma-associated herpesvirus K-bZIP protein represses transforming growth factor signal ding protein. Oncogene 2004, 23, 8272-8281. [CrossRef] [PubMed].
80. Takatsuki, K.; Matsuoka, M.; Yamaguchi, K. ATL and HTLV-1-related diseases. In Adult T-Cell Leukemia; Oxford University Press: New York, NY, USA, 1994;1-27.
81. Sugata, K.; Satou, Y.; Yasunaga, J.; Hara, H.; Ohshima, K.; Utsunomiya, A.; Mitsuyama, M.; Matsuoka, M. HTLV-1 bZIP factor impairs cell-mediated immunity by suppressing production of Th1 cytokines. Blood 2012, 119, 434-444. [CrossRef].
82. Zhao, T.; Satou, Y.; Matsuoka, M. Development of T cell lymphoma in HTLV-1 bZIP factor and Tax double transgenic mice. Arch. Virol. 2014, 159, 1849-1856. [CrossRef] [PubMed].
83. Mitagami, Y.; Yasunaga, J.; Kinosada, H.; Ohshima, K.; Matsuoka, M. Interferon- promotes inflammation and development of T-cell lymphoma in HTLV-1 bZIP factor transgenic mice. PLoS Pathog. 2015, 11, e1005120.
84. Yamamoto-Taguchi, N.; Satou, Y.; Miyazato, P.; Ohshima, K.; Nakagawa, M.; Katagiri, K.; Kinashi, T.; Matsuoka, M. HTLV-1 bZIP factor induces inflammation through labile Foxp3 expression. PLoS Pathog. 2013, 9, e1003630. [CrossRef] [PubMed].
85. Feuer, G.; Green, P.L. Comparative biology of human T-cell lymphotropic virus type 1 (HTLV-1) and HTLV-2. Oncogene 2005, 24, 5996-6004. [CrossRef] [PubMed].
86. Ciminale, V.; Rende, F.; Bertazzoni, U.; Romanelli, M.G. HTLV-1 and HTLV-2: Highly similar viruses with distinct oncogenic properties. Front. Microbiol. 2014, 5. [CrossRef] [PubMed].
87. Halin, M.; Douceron, E.; Clerc, I.; Journo, C.; Ko, N.L.; Landry, S.; Murphy, E.L.; Gessain, A.; Lemasson, I.; Mesnard, J.M. et al. Human T-cell leukemia virus type 2 produces a spliced antisense transcript encoding a protein that lacks a classic bZIP domain but still inhibits Tax2-mediated transcription. Blood 2009, 114, 2427-3248. [CrossRef].
88. Barbeau, B.; Peloponese, J.M.; Mesnard, J.M. Functional comparison of antisense proteins of HTLV-1 and HTLV-2 in viral pathogenesis. Front. Microbiol. 2013, 4. [CrossRef] [PubMed].
89. Arnold, J.; Yamamoto, B.; Li, M.; Phipps, A.J.; Younis, I.; Lairmore, M.D.; Green, P.L. Enhancement of infectivity and persistence in vivo by HBZ, a natural antisense coded protein of HTLV-1. Blood 2006, 107, 3976-3982. [CrossRef] [PubMed].
90. Yin, H.; Kannian, P.; Dissinger, N.; Haines, R.; Niewiesk, S.; Green, P.L. Human T-cell leukemia virus type 2 antisense viral protein 2 is dispensable for in vitro immortalization but functions to repress early virus replication in vivo. J. Virol. 2012, 86, 8412-8421. [CrossRef] [PubMed].