Skip to main content
SpringerLink
Log in

Restricted Vβ gene usage of tumour-infiltrating T lymphocytes in primary gastric malignant B-cell lymphoma

  • Original Article
  • Published:
Virchows Archiv Aims and scope Submit manuscript

Abstract

Ten cases of primary gastric malignant lymphoma (PGL) were investigated by immunohistochemical and molecular genetic analysis. These cases were diagnosed histopathologically as follicular small cleaved cell type (1 case), diffuse small cleaved cell type (3 cases) and diffuse large cell type (6 cases) based on the WF (Working Formulation) classification. Seven cases classified as small cleaved or diffuse large cell type belong to low (4 cases) or high (3 cases) grade MALT lymphoma according to Isaacson's classification. All PGL belonged to B lineage cells according to immunohistochemical study and immunoglobulin rearrangements. Rearrangements of TCR β chain genes were observed in four of the ten cases. The possibility that the TCR β rearrangements were caused by tumour-infiltrating T-cells (TILs) was supported by the following observations: the tumours did not show T- and B-cell biphenotype, TCR β exhibited functional VDJ rearrangement and Vβ usage pattern was not a neoplastic type. Analysis of the repertoire of the TCR β chain in TILs revealed a common usage of Vβ2 in the above four cases, and furthermore, predominant usage of a particular β chain composed of Vβ2-Dβ2.1-Jβ2.3 was observed in one of the four cases. These results indicate that the TILs of PGL have a restricted TCR repertoire.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Acha-Orbea H, Mitchell DJ, Timmermann L, Wraith DC, Tausch GS, Waldor MK, Zamvil SS, McDevitt HO, Steinman L (1988) Limited heterogeneity of T cell receptors from lymphocytes mediating autoimmune encephalomyelitis allows specific immune intervention. Cell 54:263–273

    Google Scholar 

  2. Aisenberg AC, Wilkes BM, Jacobson JO (1987) Rearrangement of the genes for the beta and gamma chains of the T cell receptor is rarely observed in adult B cell lymphoma and chronic lymphocytic leukemia. J Clin Invest 80:1209–1214

    Google Scholar 

  3. Araki A, Yumoto N, Taniguchi M, Mikata A (1994) T-cell receptor Vβ repertoires of angioimmunoblastic lymphadenopathy like T-cell lymphoma. Leukemia and Lymphoma (in press)

  4. Bahler DW, Berry G, Oksenberg J, Warnke RA, Levy R (1992) Diversity of T-cell antigen receptor variable genes used by mycosis fungoides cells. Am J Pathol 140:1–8

    Google Scholar 

  5. Boehm TL, Werle A, Drahovsky D (1987) Immunoglobulin heavy chain and T-cell receptor γ and β chain gene rearrangements in acute myeloid leukemias. Mol Biol Med 4:51–62

    Google Scholar 

  6. Bragado R, Lauzurica P, Lopez Z, Lopez de Castro A (1990) T cell receptor Vβ gene usage in human alloreactive response: Shared structural features among HLA-B27-specific T cell clones. J Exp Med 171:1189–1204

    Google Scholar 

  7. Chen Y-T, Godwin TA, Mouradian JA (1991) Immunohistochemistry and gene rearrangement studies in the diagnosis of malignant lymphomas: a comparison of 152 cases. Hum Pathol 22:1249–1257

    Google Scholar 

  8. Choi Y, Kotzin B, Herron L, Callahan J, Marrack P, Kappler J (1989) Interaction of Staphylococcus aureus toxin “superantigens” with human T cells. Proc Natl Acad Sci USA 86:8941–8945

    Google Scholar 

  9. Cleary ML, Chao J, Warnke R, Sklar J (1984) Immunoglobulin gene rearrangement as a diagnostic criterion of B-cell lymphoma. Proc Natl Acad Sci USA 81:593–597

    Google Scholar 

  10. Cossman J, Uppenkamp M, Sundeen J, Coupland R, Raffeld M (1988) Molecular genetics and the diagnosis of lymphoma. Arch Pathol Lab Med 112:117–127

    Google Scholar 

  11. Demaine AG, Ratanachaiyavong S, Pope R, Ewins D, Millward BA, McGregor AM (1989) Thyroglobulin antibodies in Grave's disease are associated with T-cell receptor beta chain and major histocompatibility complex loci. Clin Exp Immunol 77:21–24

    Google Scholar 

  12. Forster A, Hobart M, Hengartner H, Rabbitts TH (1980) An immunoglobulin heavy-chain gene is altered in two T-cell clones. Nature 286:897–899

    Google Scholar 

  13. Griesser H, Feller A, Lennert K, Minden M, Mak TW (1986) Rearrangement of the β chain of the T cell antigen receptor and immunoglobulin genes in lymphoproliferative disorders. J Clin Invest 78:1179–1184

    Google Scholar 

  14. Griesser H, Feller A, Lennert K, Tweedale M, Messner HA, Zalcberg J, Minden MD, Mak TW (1986) The structure of the T cell gamma chain gene in lymphoproliferative disorders and lymphoma cell lines. Blood 68:592–594

    Google Scholar 

  15. Griesser H, Tkachuk D, Reis MD, Mak TW (1989) Gene rearrangements and translocations in lymphoproliferative diseases. Blood 73:1402–1415

    Google Scholar 

  16. Hanson CA, Thamilarasan M, Ross CW, Stoolman LM, Schnitzer B (1990) Kappa light chain gene rearrangement in T-cell acute lymphoblastic leukemia. Am J Clin Pathol 93:563–568

    Google Scholar 

  17. Hsu SM, Raine L, Fanger H (1981) The use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedure. J Histochem Cytochem 29:577–580

    CAS  PubMed  Google Scholar 

  18. Hussel T, Isaacson PG, Crabtree JE, Spencer Jo (1993) The response of cells from low-grade B-cell gastric lymphomas of mucosa-associated lymphoid tissue to Helicobacter pylori. Lancet 342:571–574

    Google Scholar 

  19. Isaacson PG (1992) Gastrointestinal lymphomas and lymphoid hyperplasias. In: Knowles DM (ed) Neoplastic hematopathology. Williams and Wilkins, pp 953–978

  20. Kappler J, Katzin B, Herron L, Gelfand EW, Bigler RD, Boylston A, Carrel S, Posnett DN, Choi Y, Marrack P (1989) Vβ-specific stimulation of human T cells by Staphylococcal toxins. Science 244:811–813

    Google Scholar 

  21. Korsmeyer SJ, Arnold A, Bakhshi A, Ravetch JV, Siebenlist U, Hieter PA, Sharrow SO, LeBien TW, Kersey JH, Poplack DJ, Leder P, Waldmann TA (1983) Immunoglobulin gene rearrangement and cell surface antigen expression in acute lymphocytic leukemias of T cells and B cell precursor origins. J Clin Invest 71:301–313

    Google Scholar 

  22. Maniatis T, Fritsh EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  23. Miceli MC, Finn OJ (1989) T cell receptor β-chain selection in human allograft rejection. J Immunol 142:81–86

    Google Scholar 

  24. Mizutani S, Fold AM, Wiedemann LM, Chan LC, Furley AJW, Greaves MF, Molgaad HV (1986) Rearrangement of immunoglobulin heavy chain genes in human T leukaemia cells shows preferential utilization of the D segment (CD52) nearest of the J region. EMBO J 5:3467–3473

    Google Scholar 

  25. Moebius U, Manns M, Hess G, Kober G, Meyer BK, Meuer SC (1990) T cell receptor gene-rearrangements of T lymphocytes infiltrating the liver in chronic active hepatitis B and primary biliary cirrhosis (PBC): oligoclonality of PBC-derived T cell clones. Eur J Immunol 20:889–896

    Google Scholar 

  26. Moller DR, Konishi K, Kirby M, Balbi B, Crystal RG (1988) Bias toward use of a specific T cell receptor β-chain variable region in a subgroup of individuals with sarcoidosis. J Clin Invest 82:1183–1191

    Google Scholar 

  27. Nitta T, Oksenberg JR, Rao NA, Steinman L (1990) Predominant expression of T cell receptor Vα7 in tumor infiltrating lymphocytes of uveal melanoma. Science 249:672–674

    Google Scholar 

  28. Nitta T, Sato K, Okumura K, Steinman L (1991) An analysis of T-cell-receptor variable-region genes in tumor-infiltrating lymphocytes within malignant tumors. Int J Cancer 49:545–550

    Google Scholar 

  29. Oksenberg JR, Stuart S, Begovich AB, Bell RB, Erlich HA, Steinman L, Bernard CCA (1990) Limited heterogeneity of rearranged T-cell receptor Vα transcripts in brains of multiple sclerosis patients. Nature 345:344–346

    Google Scholar 

  30. Pelicci P-G, Knowles DM, Dalla-Favera R (1985) Lymphoid tumors displaying rearrangements of both immunoglobulin and T-cell receptor genes. J Exp Med 162:1015–1024

    Google Scholar 

  31. Posnett DN, Schmelkin I, Burton DA, August A, McGrath H, Mayer LF (1990) T cell antigen receptor V gene usage. Increases in Vβ8+ T cell in Crohn's disease. J Clin Invest 85:1770–1776

    Google Scholar 

  32. Robinson MA (1991) The human T cell receptor β-chain gene complex contains at least 57 variable gene segments. Identification of six Vβ genes in four new gene families. J Immunol 146:4392–4397

    Google Scholar 

  33. Sanger F, Nichlen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    CAS  PubMed  Google Scholar 

  34. Sheibani K, Wu A, Ben-Ezra J, Stroup R, Rappaport H, Winberg C (1987) Rearrangement of κ-chain and T-cell receptor β chain genes in malignant lymphomas of T-cell phenotype. Am J Pathol 129:201–207

    Google Scholar 

  35. Sumida Y, Yonaha F, Maeda E, Tanabe E, Koike T, Tomioka H, Yoshida S (1992) T cell receptor repertoire of infiltrating T cells in lip of Sjörgren's syndrome patients. J Clin Invest 89:681–685

    Google Scholar 

  36. Suzuki M, Koseki H, Mizutani Y, Kuribayashi K, Kanno M, Taniguchi M (1992) Expansion of murine T cells bearing a unique T cell receptor beta-chain in Friend virus-induced tumor in situ. J Immunol 148:2968–2973

    Google Scholar 

  37. Tawa A, Hozumi N, Minden M, Mak TW, Gelfaurd EW (1986) Rearrangement of the T-cell receptor β-chain gene in non-T, non-B acute lymphoblastic leukemia of childhood. N Engl J Med 313:1033–1037

    Google Scholar 

  38. Teng WP, Cohen SB, Posnett DN, Weetman AP (1990) T cell receptor phenotypes in autoimmune thyroid disease. J Endocrinol Invest 13:339–342

    Google Scholar 

  39. The non-Hodgkin's lymphoma pathologic classification project (1982) National Cancer Institute sponsored study of classifications of non-Hodgkin's lymphoma: summary and description of a working formulation for clinical usage. Cancer 49:2112–2135

    Google Scholar 

  40. Tkachuk DC, Griesser H, Takihara E, Champagne E, Minden M, Feller AC, Lennert K, Mak TW (1988) Rearrangement of T-cell locus in lymphoproliferative disorders. Blood 72:353–357

    Google Scholar 

  41. Yanagi Y, Maekawa R, Cook T, Kanagawa O, Oldstone MB (1990) Restricted V-segment usage in T-cell receptors from cytotoxic T lymphocytes specific for a major epitope of lymphocytic choriomeningitis virus. J Virol 64:5919–5926

    Google Scholar 

  42. Zamvil SS, Mitchell DJ, Lee NE, Moore AC, Waldor MK, Sakai K, Rothbard JB, McDevitt HO, Steinman L, Acha-Orbea H (1988) Predominant expression of a T cell receptor Vβ gene subfamily in autoimmune encephalomyelitis. J Exp Med 167:1586–1596

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. 1st Department of Pathology, School of Medicine, Chiba University, 1-8-1 Inohana, Chuo-ku, 260, Chiba City, Chiba, Japan

    N. Yumoto, A. Araki & A. Mikata

  2. Second Department of Internal Medicine, School of Medicine, Chiba University, Chiba, Japan

    T. Sumida

  3. Division of Molecular Genetics, Center for Biomedical Science, School of Medicine, Chiba University, Chiba, Japan

    T. Saito

  4. Division of Molecular Immunology, Center for Biomedical Science, School of Medicine, Chiba University, Chiba, Japan

    M. Taniguchi

Authors
  1. N. Yumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Araki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Mikata
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Sumida
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Taniguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yumoto, N., Araki, A., Mikata, A. et al. Restricted Vβ gene usage of tumour-infiltrating T lymphocytes in primary gastric malignant B-cell lymphoma. Vichows Archiv A Pathol Anat 426, 11–18 (1995). https://doi.org/10.1007/BF00194693

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00194693

Key words

Search

Navigation