Random suppression of T cells that bear specific T cell receptor Vβ sequences in adult T cell leukemia/lymphoma (ATLL) patients at each clinical stage: Carrier, smoldering, chronic, and acute
Corresponding Author
Koichi Ohshima
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Department of Pathology, School of Medicine, Fukuoka University, Nanakuma 7-45-1, Jonan-ku, Fukuoka 814-01, JapanSearch for more papers by this authorJunji Suzumiya
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorMasahiro Kikuchi
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorMorishige Takeshita
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorKotaro Tashiro
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorNobuhiro Kimura
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorCorresponding Author
Koichi Ohshima
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Department of Pathology, School of Medicine, Fukuoka University, Nanakuma 7-45-1, Jonan-ku, Fukuoka 814-01, JapanSearch for more papers by this authorJunji Suzumiya
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorMasahiro Kikuchi
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorMorishige Takeshita
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorKotaro Tashiro
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorNobuhiro Kimura
Department of Pathology, and First Internal Medicine, School of Medicine, Fukuoka University, Fukuoka, Japan
Search for more papers by this authorAbstract
Human T cell leukemia virus type I (HTLV-I) is associated with adult T cell leukemia/lymphoma (ATLL), which is well known as a T cell malignancy. In order to clarify whether HTLV-I plays a role as a virus-encoded superantigen in the neoplastic process, we examined the TCR Vβ families in the peripheral blood at four different clinical stages: carrier, smoldering leukemia, chronic leukemia, and acute leukemia. An increased number of CD4 T cells was found in each of the four clinical stages. However, we found neither uniform specific losses nor uniform clonal expansion of particular TCR Vβ gene families in any case from the four clinical stages. However, a suppression of the random TCR Vβ families was found. Our data did not therefore directly suggest the existence of a common superantigen model of HTLV-I which induces an increase in CD4 T cells. The random suppression in the TCR Vβ repertoire is most likely caused by the influence of HTLV-I neoplastic pathogenesis rather than by virus-encoded superantigens. In the patients with acute leukemia, one or two families of the Vβ repertoires were very strongly expressed, while in chronic leukemia, no such repertoire of strong expression was observed. The immunological reaction of the hosts might thus be different between the above described groups. © 1996 Wiley-Liss, Inc.
References
- 1 Shimoyama M, Minato K, Saito H, Kitahara T, Kond C, Nakazawa M, Ishihara K, Watanabe S, Inada N, Nagatani T, Deura K, Mikata A: Comparison of clinical, morphologic and immunologic characteristics of adult T-cell leukemia-lymphoma and cutaneous T-cell lymphoma. J Clin Oncol 9: 357–372, 1979.
- 2 Uchiyama T, Yodoi J, Sagawa K, Takatsuki K, Uchino H: Adult T-cell leukemia. Clinical and hematologic features of 16 cases. Blood 50: 481–492, 1977.
- 3 Yamaguchi K, Yoshida R, Kiyokawa T, Seiki M, Yoshida M, Takatsuki K: Lymphoma type adult T-cell leukemia A clinico-pathologic study of HTLV related T-cell type malignant lymphoma. Hematol Oncol 4: 59–65, 1986.
- 4 Takatsuki K: Overview of adult T-cell leukemidlymphoma. Jpn Soc Res 25: 97–103, 1985.
- 5 Yoshida M, Seiki M, Yamaguchi K, Takatsuki K: Monoclonal integra-tion of human T-cell leukemia provirus in all primary tumors of adult T-cell leukemia suggests causative role of human T-cell leukemia virus in the disease. Proc Natl Acad Sci USA 81: 2534–2537, 1984.
- 6 Ohshima K, Yoshida T, Kikuchi M, Masuda Y, Kimura N, Satoh H: Rearrangement of human T cell receptor beta and gamma genes in adult T cell leukemia/lymphoma. Hematol Oncol 8: 111–118, 1990.
- 7
Kawano F,
Yamaguchi K,
Nishimura H,
Tsuda H,
Takatsuki K:
Variation in the clinical courses of adult T-cell leukemia.
Cancer
55: 851–856,
1985.
10.1002/1097-0142(19850215)55:4<851::AID-CNCR2820550424>3.0.CO;2-J PubMed Web of Science® Google Scholar
- 8 Wucherpfennig KW, Ota K, Endo N, Seidman JG, Rosenzweig A, Weiner HL, Hafler DA: Shared human T-cell receptor Vβ usage to immunodominant regions of myelin basic protein. Science 248: 1016–1019, 1990.
- 9 Marrack P, Kappler J: The staphyloccocal enterotoxins and their relatives. Science 248: 705–711, 1990.
- 10 Boldt-Houle DM, Rinaldo CR, Ehrlich GD: Random depletion of T cells that bear specific T cell receptor Vβ sequences in AIDS patients. J Leukoc Biol 54: 48–91, 1993.
- 11
Ohshima K,
Kikuchi M,
Masuda Y,
Sumiyoshi Y,
Eguchi F,
Mohtai H,
Takeshita M,
Kimura N:
Human T-cell leukemia virus type I associated lymphadenitis.
Cancer
69: 239–248,
1992.
10.1002/1097-0142(19920101)69:1<239::AID-CNCR2820690139>3.0.CO;2-# PubMed Web of Science® Google Scholar
- 12 Seiki M, Hattori S, Hirayama Y, Yoshida M: Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci USA 80: 3618–3622, 1983.
- 13 Sottini A, Imberti L, Gorla R, Cattaneo R, Primi D: Restricted expres-sion of T cell receptor Vβ but not Vol genes in rheumatoid arthritis. Eur J Immunol 21: 461–466, 1991.
- 14 Kinoshita T, Shimoyama M, Tobinai K, Ito M, Ito S, Ikeda S, Tajima K, Shimotohno K: Detection of mRNA for texl/rexl gene of human T-cell leukemia virus type I in fresh peripheral blood mononuclear cells of adult T-cell leukemia patients and viral carriers by using the polymerase chain reaction. Proc Natl Acad Sci USA 86: 5620–5624, 1989.
- 15 Takatsuki K, Yamaguchi K, Watanabe T, Mochizuki M, Kiyokawa T, Mori S, Miyata N: Adult T-cell leukemia and HTLV-I related diseases. Gann Mono Can Res 39: 1–15, 1992.
- 16 Cross SL, Feinberg MB, Wolf JB, Holbrook NJ, Wong-Staal F, Leonard WJ: Regulation of the human interleukin-2 receptor alpha chain promoter: activation of a nonfunctional promoter by the transactivator gene of HTLV-I. Cell 49: 47–56, 1987.
- 17 Maruyama M, Shibuya H, Harada H, Hatakeyama M, Seiki M, Fujita T, Inoue J, Yoshida M, Taniguchi T Evidence for aberrant activation of the interleukin-2 autocrine loop by HTLV-1-encoded p40x and T3/Ti complex triggering. Cell 48: 343–350, 1987.
- 18 Yoshida M: Expression of the HTLV-1 genome and its association with aunique T-cell malignancy. Biochim Biophys Acta 907: 145–161, 1987.
- 19 Franchin G, Wong-Staal F, Gallo RC: Human T-cell leukemia virus (HTLV-I) transcripts in fresh and cultured cells of patients with adult T-cell leukemia. Proc Natl Acad Sci USA 81: 6207–6211, 1984.
- 20 Concannon P, Pickering LA, Kung P, Hood L: Diversity and structure of human T-cell receptor Vβ chain variable region genes. Proc Natl Acad Sci USA 83: 6598–6602, 1986.
- 21 Kimura N, Toyonaga B, Yoshikai Y, Du RP, Mak TW Sequences and repertoire of the human T cell receptor α and β chain variable region genes in thymocytes. Eur J Immunol 17: 375–383, 1987.
- 22 Fleischer B, Schrezenmeier H: T cell stimulation by staphylococcal enterotoxins. enterotoxins. Clonal variable response and requirements for major his-tocompatibility complex class I1 molecules on accessory or target cells. J Exp Med 167: 1697–1707, 1988.
- 23 Kappler J, Kotzin B, Herron L, Gelfand EW, Bigler RB, Boylston A. Carrel S, Posnett DN, Choi Y, Marrack P: VP-specific stimulation of human T cells by staphylococcal toxins. Science 244: 811–813, 1989.
- 24 Imberti L, Sottini A, Bettinardi A, Puoto M, Primi D: Selective depletion in HIV infection of T cells that bear specific T cell receptor Vβ sequences. Science 254: 860–862, 1991.
- 25 Boyer V, Smith LR, Ferre F, Pezzoli P, Trauger RJ, Jensen FC, Carlo DJ: T cell receptor Vβ repertoire in HIV-infected individuals: lack of evidence for selective Vβ deletion. Clin Exp Immunol 92: 437–441, 1993.
- 26 Kimata JT, Wong FH, Ratner L: CD3-dependent lymphocyte activation by human T cell leukemia virus type I-producing T cells. J Gen Virol 75: 2433–2437, 1994.
- 27
Clark DM,
Boylston AW,
Hall PA,
Carrel S:
Antibodies to T cell antigen receptor beta chain families detect monoclonal T cell prolifera-tion
Lancet
ii: 835–838,
1986.
10.1016/S0140-6736(86)92870-9 Google Scholar
- 28 Preesman AH, Hu HZ, Tilanus MGJ, de Geus B, Schuurman HJ, Reitsma R, van Wichen DF, van Vloten WA, de Weger RA: T cell receptor Vβ-family usage in primary cutaneous and primary nodal T-cell non-Hodgkins lymphomas. J Invest Dermatol 99: 587–593, 1992.
- 29 Jack AS, Boylston AW, Carrel S, Grigor I: Cutaneous T-cell lymphoma cells employ a restricted range of T-cell antigen receptor variable region genes. Am J Pathol 136: 17–21, 1990.
- 30 Kannagi M, Harada S, Maruyama I, Inoko H, Igarashi H, Kuwashima G, Sato S, Morita M, Kidokoro M, Sugimoto M, Funahashi S, Osame M, Shida H: 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 8: 761–767, 1991.
- 31 Kannagi M, Shida H, Igarashi H, Kuruma K, Murai H, Aono Y, Maru-yama I, Osame M, Hattori T, Inoko H, Harada S: Target epitope in the tax protein of human T-cell leukemia virus type I recognized by class I major histocompatibility complex-restricted cytotoxic T cells. J Virol 66: 2928–2933, 1992.