Цель: определить показания и последовательность проведения молекулярных исследований при ангиоиммунобластной Т-клеточной лимфоме (АИТЛ) в различном биологическом материале. Материалы и методы. Молекулярные исследования проведены у 84 первичных больных АИТЛ. Медиана возраста составила 61 (29–81) год, соотношение мужчины/женщины – 48/36. Оценку T-клеточной и В-клеточной клональности проводили по реаранжировкам генов цепей T-клеточного рецептора и тяжелых цепей иммуноглобулинов. Для количественного определения клеток с мутацией G17V гена RHOA применяли полимеразную цепную реакцию (ПЦР) в реальном времени с аллель-специфичными LNA модифицированными праймерами. Результаты. В биоптатах лимфатических узлов реаранжировки генов цепей Т-клеточных рецепторов определены у 76 (90,5%) из 84 больных и отсутствовали в 8 (9,5%) случаях. Выявление одинаковых клональных продуктов амплификации генов TCRG и TCRB в биоптате лимфатического узла и в образцах периферической крови и/или костного мозга свидетельствовало о лейкемизации опухолевого процесса и наблюдалось у 64,7% больных. Определение в образцах периферической крови и/или костного мозга клональных продуктов, отсутствующих в лимфатическом узле, обусловлено реактивной цитотоксической популяцией лимфоцитов и наблюдалось в 58,8% случаев АИТЛ. Одновременное выявление Т- и В-клеточной клональности в биоптате лимфатического узла отмечалось у 20 (24,7%) из 81 больного. Клетки с мутацией G17V гена RHOA выявлены в биоптатах лимфоузлов у 45 (54,9%) из 82 пациентов. Применение метода аллель-специфичной ПЦР с LNA модифицированными праймерами позволило выявить лейкемизацию опухолевого процесса у 100% и поражение костного мозга – у 93,9% пациентов с выявленной мутацией в лимфоузлах. Заключение. В результате выполненной работы определены показания и последовательность проведения молекулярных исследований при АИТЛ в различном биологическом материале. Количественная аллель-специфичная ПЦР с LNA модифицированными праймерами для определения мутации G17V гена RHOA обладает высокой чувствительностью, позволяет верифицировать лейкемизацию опухолевого процесса и проводить мониторинг минимальной резидуальной болезни во время терапии.
Aim: to determine molecular diagnostics routine for different tissue samples in angioimmunoblastic T-cell lymphoma. Materials and methods. Molecular studies were performed for 84 primary AITL patients. The median age was 61 year (29–81); the male to female ratio was 48/36. T-cell and B-cell clonality was assessed by GeneScan analysis of rearranged T-cell receptor (TCRG, TCRB) and immunoglobulin heavy chain genes. For the quantitative determination of cells with RHOA G17V mutation real-time polymerase chain reaction (PCR) with allele-specific LNA modified primers was used. Results. In lymph nodes rearrangements of T-cell receptor genes were determined in 76 (90.5%) of 84 patients and were absent in 8 (9.5%) cases. Identification of the same clonal products of the TCRG and TCRB genes in the lymph node and in peripheral blood and/or bone marrow indicated the prevalence of the tumor process and was observed in 64.7% of patients. Clonal products in peripheral blood and/or bone marrow different from those in the lymph node indicated reactive cytotoxic lymphocyte population and were noted in 58.8% of AITL cases. Simultaneous detection of T- and B-cell clonality in the lymph node was observed in 20 (24.7%) of 81 patients. Cells with RHOA G17V mutation were detected in lymph node in 45 (54.9%) of 82 patients. The use of allele-specific PCR with LNA modified primers revealed presence of the tumor cells in peripheral blood in 100% and in bone marrow in 93.9% of patients with G17V RHOA mutation in the lymph nodes. Conclusion. The validity of different molecular assays performed on certain tissue samples for the diagnosis of angioimmunoblastic T-cell lymphoma has been evaluated. Quantitative allele-specific PCR assay for RHOA G17V mutation based on LNA modified primers possesses sufficient sensitivity for tumor process prevalence evaluation and minimal residual disease monitoring.
Keywords: T-cell receptor and immunoglobulin heavy chains genes rearrangements, RHOA G17V mutation, angioimmunoblastic T-cell lymphoma.
Список литературы
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________________________________________________
1. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Arber DA, Hasserjian RP, LeBeau MM, Orazi A, Siebert R. WHO classification of tumors of haematopoietic and lymphoid tissues. Lyon: IARC, 2017:407-10.
2. Frizzera G, Moran EM, Rappaport H. Angioimmunoblastic lymphadenopathy with dysproteinaemia. Lancet. 1974;1:1070-3.
3. Lukes RJ, Tindle BH. Immunoblastic lymphadenopathy. A hyperimmune entity resembling Hodgkin's disease. N Engl J Med. 1975;292(1):1-8.
4. Frizzera G, Moran EM, Rappaport H. Angio-immunoblastic lymphadenopathy: diagnosis and clinical course. Am J Med.1975;59:803-18.
5. Willenbrock K, Renné C, Gaulard P, Hansmann ML. In angioimmunoblastic T-cell lymphoma, neoplastic T cells may be a minor cell population. A molecular single-cell and immunohistochemical study. Virchows Arch. 2005;446(1):15-20. doi: 10.1007/s00428-004-1114-1
6. de Leval L, Gisselbrecht C, Gaulard P. Advances in the understanding and management of angioimmunoblastic T-cell lymphoma. Br J Haematol. 2010;148(5):673-89. doi: 10.1111/j.1365-2141.2009.08003.x
7. Weiss LM, Jaffe ES, Liu XF, Chen YY, Shibata D, Medeiros LJ. Detection and localization of Epstein-Barr viral genomes in angioimmunoblastic lymphadenopathy and angioimmunoblastic lymphadenopathy-like lymphoma. Blood. 1992;79:1789-95.
8. Dogan A, Attygalle AD, Kyriakou C. Angioimunoblastic T-cell lymphoma. Br J Haematol. 2003;121:681-91.
9. [Stefanov DN, Kovrigina AM, Poddubnaya AM. A new concept of angioimmunoblastic T-cell lymphoma origin: from molecular biology to therapy. Bulleten SO RAMN. 2011;31(2):14-9 (In Russ.)].
10. Dupuis J, Boye K, Martin N, Copie-Bergman C, Plonquet A, Fabiani B, Baglin AC, Haioun C, Delfau-Larue MH, Gaulard P. Expression of CXCL13 by neoplastic cells in angioimmunoblastic T-cell lymphoma (AITL). A new diagnostic marker providing evidence that AITL derives from follicular helper T-cells. Am J Surg Pathol. 2006;30:490-4.
11. Lachenal F, Berger F, Ghesquières H, Biron P, Hot A, Callet-Bauchu E, Chassagne C, Coiffier B, Durieu I, Rousset H, Salles G. Angioimmunoblastic T-cell lymphoma: clinical and laboratory features at diagnosis in 77 patients. Medicine (Baltimore). 2007;86(5):282-92. doi: 10.1097/MD.0b013e3181573059
12. [Chernova NG, Vinogradova YuE, Sidorova YuV, Kaplanskaya IB, Gilyazitdinova EA, Gorenkova LG, Mar'in DS, Kremenetskaya AM, Vorob'ev AI, Kravchenko SK. Prolonged chemotherapy for angioimmunoblastic T-cell lymphoma. Russian Journal of klinicheskaya onkogematologiya. Fundamental'nye issledovaniya i klinicheskaya praktika. 2014;7(1):57-62 (In Russ.)].
13. Tan BT, Warnke RA, Arber DA. The frequency of B- and T-cell gene rearrangements and Epstein-Barr virus in T-cell lymphomas: a comparison between angioimmunoblastic T-cell lymphoma and peripheral T-cell lymphoma, unspecified with and without associated B-cell proliferations. J Mol Diagn. 2006;8(4):466-75. doi: 10.2353/jmoldx.2006.060016
14. [Sidorova YuV, Nikulina EE, Chernova NG, Gorenkova LG, Gilyazitdinova EA, Kravchenko SK, Kovrigina AM, Sudarikov AB. PCR-based clonality detection in angioimmunoblastic T-cell lymphoma. Russian Journal of klinicheskaya onkogematologiya. Fundamental'nye issledovaniya i klinicheskaya praktika. 2014;7(2):192-6 (In Russ.)].
15. [Chernova NG, Sidorova YuV, Zakharko EI, Naumova EV, Ryzhikova NV, Galtseva IV, Dvirnyk VN, Smirnova SYu, Sudarikov AB, Kokhno AV, Moiseeva TN, Lugovskaya SA, Zvonkov EE, Savchenko VG. Flow cytometry and PCR-based T-cell clonality testing for discriminating between reactive and neoplastic proliferation of large granular lymphocytes. Russian Journal of Hematology and Transfusiology (Gematologiya i transfusiologiya). 2018; 2:124-33 (In Russ.)]. doi: 10.25837/HAT.2018.48..2..003
16. [Sidorova YuV, Nikitin EA, Melikyan AL, Pivnik AV, Sudarikov AB. Use of PCR-SSCP-TCRy method to determine T-cell clonality in infectious mononucleosis. Russian Journal of Hematology and Transfusiology (Gematologiya i transfusiologiya). 2004;49(6):1-7 (In Russ.)].
17. Smirnova SJ, Sidorova JV, Tsvetaeva NV, Nikulina OF, Biderman BV, Nikulina EE, Kulikov SM, Sudarikov AB. Expansion of CD8+ cells in autoimmune hemolytic anemia. Autoimmunity. 2016;49(3):147-54. doi: 10.3109/08916934.2016.1138219
18. Sakata-Yanagimoto M, Enami T, Yoshida K, Shiraishi Y, Ishii R, Miyake Y, Muto H, Tsuyama N, Sato-Otsubo A, Okuno Y, Sakata S, Kamada Y, Nakamoto-Matsubara R, Tran NB, Izutsu K, Sato Y, Ohta Y, Furuta J, Shimizu S, Komeno T, Sato Y, Ito T, Noguchi M, Noguchi E, Sanada M, Chiba K, Tanaka H, Suzukawa K, Nanmoku T, Hasegawa Y, Nureki O, Miyano S, Nakamura N, Takeuchi K, Ogawa S, Chiba S. Somatic RHOA mutation in angioimmunoblastic T-cell lymphoma. Nat Genet. 2014;46(2):171-5. doi: 10.1038/ng.2872
19. Nakamoto-Matsubara R, Sakata-Yanagimoto M, Enami T, Yoshida K, Yanagimoto S, Shiozawa Y, Nanmoku T, Satomi K, Muto H, Obara N, Kato T, Kurita N, Yokoyama Y, Izutsu K, Ota Y, Sanada M, Shimizu S, Komeno T, Sato Y, Ito T, Kitabayashi I, Takeuchi K, Nakamura N, Ogawa S, Chiba S. Detection of the G17V RHOA mutation in angioimmunoblastic T-cell lymphoma and related lymphomas using quantitative allele-specific PCR. PLoS One. 2014;9(10):e109714. doi: 10.1371/journal.pone.010 9714
20. Kataoka K, Ogawa S. Variegated RHOA mutations in human cancers. Exp Hematol. 2016;44(12):1123-9. doi: 10.1016/j.exphem.2016.09.002
21. Manso R, González-Rincón J, Rodríguez-Justo M, Roncador G, Gоmez S, Sánchez-Beato M, Piris MA, Rodriguez-Pinilla SM. Overlap at the molecular and immunohistochemical levels between angioimmunoblastic T-cell lymphoma and a subgroup of peripheral T-cell lymphomas without specific morphological features. Oncotarget. 2018;9(22):16124-33. doi: 10.18632/oncotarget.24592
22. Dongen JJ, Langerak AW, Bruggemann M, Evans PA, Hummel M, Lavender FL, Delabesse E, Davi F, Schuuring E, Garcia-Sanz R, Krieken JH, Droese J, Gonzalez D, Bastard C, White HE, Spaargaren M, Gonzalez M, Parreira A, Smith JL, Morgan GJ, Kneba M, Macintyre EA. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia. 2003;17(12):2257-317. doi: 10.1038/sj.leu.2403202
23. Sidorova YuV, Chernova NG, Sinitsyna MN, Aleksenko MY, Glinshchikova OA, Smirnova SYu, Ryzhikova NV, Nikulina EE, Zakharko EI, Rybkina EB, Dvirnyk VN, Kovrigina AM, Zvonkov EE, Sudarikov AB. Monitoring of RHOA G17V mutation during the course of therapy in patients with angioimmunoblastic T-cell lymphoma by quantitative allele-specific PCR with LNA-modified primers. Hemasphere. Abstract book. 23rd Congress of the European Hematology Association. 2018;2(S):89-90.
24. Smirnova S, Sidorova Y, Chernova N, Zvonkov E, Sinitsyna M, Sychevskaya K, Glinshchikova O, Ryzhikova N, Kovrigina A, Sudarikov A. CD8+ T-cell clones persistent in bone marrow and peripheral blood during course of CD4+ angioimmunoblastic T-cell lymphoma. Haematologica. 2017;102(suppl 1):578, E1403.
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26. Higgins JP, van de Rijn M, Jones CD, Zehnder JL, Warnke RA. Peripheral T-cell lymphoma complicated by a proliferation of large B-cells. Am J Clin Pathol. 2000;114:236-47.
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