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. 1998 Oct;153(4):1229-37.
doi: 10.1016/S0002-9440(10)65667-2.

Human interleukin-10 expression in T/natural killer-cell lymphomas: association with anaplastic large cell lymphomas and nasal natural killer-cell lymphomas

M L Boulland  1 , V Meignin, K Leroy-Viard, C Copie-Bergman, J Brière, R Touitou, P Kanavaros, P Gaulard
Affiliations

Human interleukin-10 expression in T/natural killer-cell lymphomas: association with anaplastic large cell lymphomas and nasal natural killer-cell lymphomas

M L Boulland et al. Am J Pathol. 1998 Oct.

Abstract

Several cytokines have been implicated in the pathogenesis of human lymphomas. Among them, interleukin-10 (IL-10) is a pleiotropic cytokine with various biological effects on B and T lymphocytes. Its expression has been essentially studied in B-cell lymphomas, where it appears to act as an autocrine growth factor. BCRF1 (also called viral IL-10), an open reading frame of Epstein-Barr virus, exhibits extensive sequence and functional homologies with human IL-10. Some entities belonging to T- or natural killer (NK)-cell lymphomas are characterized by a frequent association with Epstein-Barr virus. We analyzed 39 cases of peripheral T-cell lymphoma, as well as 7 cases of nasal NK-cell lymphoma, for the presence of IL-10 transcripts by in situ hybridization, to see whether this cytokine was expressed in these tumors and whether its expression could be related to their histological subtype and to the presence of Epstein-Barr virus. Because the riboprobe used for in situ hybridization recognizes both human and viral IL-10, 12 cases were also analyzed by reverse transcription-polymerase chain reaction to verify the human or viral origin of IL-10. It was found that 8 of 11 (73%) anaplastic large cell lymphomas (ALCLs), 2 of 11 (18%) pleomorphic T-cell lymphomas, and 3 of 7 (43%) nasal NK-cell lymphomas exhibited a large number of IL-10-expressing cells, whereas only rare scattered cells were detected in angioimmunoblastic (11 of 11) and in gammadelta T-cell lymphomas (6 of 6). In ALCLs, the pattern of IL-10 mRNA-expressing cells showed an overlapping with the CD30 staining and preferential localization in sinusal and perifollicular areas, thereby suggesting that IL-10-expressing cells were tumor cells. Furthermore, IL-10 transcripts were detected in the SU-DHL-1 anaplastic lymphoma cell line. No correlation with Epstein-Barr virus profile was found, because all cases of ALCL were negative for EBER 1 and 2 genes by in situ hybridization. We confirmed the presence of human IL-10 mRNA by reverse transcription-polymerase chain reaction in ALCLs as well as in NK-cell lymphomas, whereas viral IL-10 was not detected. Thus, human and not viral IL-10 is frequently expressed by tumor cells in ALCLs and nasal NK-cell lymphomas. In view of its function in the proliferation and the differentiation of cytotoxic T and NK cells, and its immunosuppressive properties, IL-10 may have a role in the pathogenesis of these lymphomas.

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Figures

Figure 1.
Figure 1.
IL-10 mRNA expression detected by ISH in NK-cell lymphomas and in T-cell lymphomas of different histological subtypes. Results are shown as IL-10-positive cells/mm of tissue sections.
Figure 2.
Figure 2.
Nasal NK-cell lymphoma (case 44). Numerous cells strongly expressed IL-10 mRNA by ISH (A), with a similar pattern of latent membrane protein (LMP) expression by immunohistochemistry (alkaline phosphatase-anti-alkaline phosphatase technique; B).
Figure 3.
Figure 3.
IL-10 mRNA expression in ALCL and the SU-DHL-1 cell line. Overlapping pattern in a sinusal area (case 32) was shown for IL-10 mRNA expression by ISH with a radiolabeled probe (A) and CD30 staining by immunohistochemistry (alkaline phosphatase-anti-alkaline phosphatase technique; B). C: IL-10 mRNA expression by ISH with a digoxigenin-labeled probe on paraffin sections in the same case demonstrates IL-10 mRNA staining detected in the cytoplasm of large anaplastic cells with kidney-shaped nuclei. D: IL-10 transcripts were detected in cells of the SU-DHL-1 cell line by ISH with a radiolabeled probe.
Figure 4.
Figure 4.
RT-PCR analysis for the expression of hIL-10 and vIL-10/BCRF1 in NK-cell lymphomas (lanes 3 to 7). SU-DHL-1 and B95-8 cell lines were used as positive controls for hIL-10 and vIL-10/BCRF1, respectively (lanes 1 and 2). Omission of cDNA in all reverse transcription reactions was used as negative control. The S14 gene was used as a control for the quality and quantity of total RNAs.
Figure 5.
Figure 5.
RT-PCR analysis for the expression of hIL-10 and vIL-10/BCRF1 in PTCLs: PML (lanes 3 to 5), AILD (lanes 6 and 7), and ALCL (lanes 8 and 9). The SU-DHL-1 and B95-8 cell lines were used as positive controls for hIL-10 and vIL-10/BCRF1, respectively (lanes 1 and 2). Omission of cDNA in all reverse transcription reactions was used as a negative control. The S14 gene was used as control for the quality and quantity of total RNAs.
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