The reliability of immunohistochemical analysis of the tumor microenvironment in follicular lymphoma: A validation study from the Lunenburg Lymphoma Biomarker Consortium

Haematologica

Volumn 99, Issue 4, 2014, Pages 715-725

  Sander, Birgitta ^a   de Jong, Daphne ^b   Rosenwald, Andreas ^c   Xie, Wanling ^d   Balagué, Olga ^b   Calaminici, Maria ^e   Carreras, Joaquim ^f,q   Gaulard, Philippe ^g   Gribben, John ^e   Hagenbeek, Anton ^h   Kersten, Marie José ^h   Molina, Thierry Jo ⁱ   Lee, Abigail ^e   Montes Moreno, Santiago ^j   Ott, German ^k   Raemaekers, John ^l   Salles, Gilles ^m   Sehn, Laurie ⁿ   Thorns, Christoph ^o   Wahlin, Björn E ^p   Gascoyne, Randy D ⁿ   Weller, Edie ^d   more..

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b ANTONI VAN LEEUWENHOEK HOSPITAL   (Netherlands)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d DANA FARBER CANCER INSTITUTE   (United States)

^e QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^f UNIVERSITY OF BARCELONA   (Spain)

^g HENRI MONDOR HOSPITAL   (France)

^h ACADEMIC MEDICAL CENTER   (Netherlands)

ⁱ UNIVERSITÉ PARIS DESCARTES   (France)

^j HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^k ROBERT BOSCH HOSPITAL   (Germany)

^l RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^m UNIVERSITÉ LYON 1   (France)

ⁿ UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^o UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^p KAROLINSKA INSTITUTE   (Sweden)

^q TOKAI UNIVERSITY   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD34 ANTIGEN; CD4 ANTIGEN; CD68 ANTIGEN; CD8 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; KI 67 ANTIGEN; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; TUMOR MARKER;

ARTICLE; CANCER PROGNOSIS; CELL INFILTRATION; FLOW CYTOMETRY; FOLLICULAR LYMPHOMA; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MICROSCOPY; REPRODUCIBILITY; SCORING SYSTEM; TISSUE MICROARRAY; TUMOR MICROENVIRONMENT; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; PATHOLOGY; T LYMPHOCYTE SUBPOPULATION; TUMOR ASSOCIATED LEUKOCYTE;

ANTIGENS, CD; BIOMARKERS, TUMOR; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; LYMPHOCYTES, TUMOR-INFILTRATING; LYMPHOMA, FOLLICULAR; REPRODUCIBILITY OF RESULTS; T-LYMPHOCYTE SUBSETS; TUMOR MICROENVIRONMENT;

EID: 84897402974     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2013.095257     Document Type: Article

References (44)

1. Pulte D, Jansen L, Gondos A, Emrich K, Holleczek B, Katalinic A, et al. Survival of patients with non-Hodgkin lymphoma in Germany in the early 21st century. Leuk Lymphoma. 2012;54(5):979-85.
2. Pulte D, Gondos A, Brenner H. Expected long-term survival of older patients diagnosed with non-Hodgkin lymphoma in 2008-2012. Cancer Epidemiol. 2012;36(1): e19-25.
3. Horning SJ, Rosenberg SA. The natural history of initially untreated low-grade non-Hodgkin's lymphomas. N Engl J Med. 1984;311(23):1471-5.
4. Rohatiner AZ, Lister TA. The clinical course of follicular lymphoma. Best Pract Res Clin Haematol. 2005;18(1):1-10.
5. Solal-Celigny P, Cahu X, Cartron G. Follicular lymphoma prognostic factors in the modern era: what is clinically meaningful? Int J Hematol. 2010;92(2):246-54.
6. Relander T, Johnson NA, Farinha P, Connors JM, Sehn LH, Gascoyne RD. Prognostic factors in follicular lymphoma. J Clin Oncol. 2010;28(17):2902-13.
7. Solal-Celigny P, Roy P, Colombat P, White J, Armitage JO, Arranz-Saez R, et al. Follicular lymphoma international prognostic index. Blood. 2004;104(5):1258-65.
8. Federico M, Bellei M, Marcheselli L, Luminari S, Lopez-Guillermo A, Vitolo U, et al. Follicular lymphoma international prognostic index 2: a new prognostic index for follicular lymphoma developed by the international follicular lymphoma prognostic factor project. J Clin Oncol. 2009;27(27):4555-62.
9. Dave SS, Wright G, Tan B, Rosenwald A, Gascoyne RD, Chan WC, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med. 2004;351(21): 2159-69.
10. Glas AM, Knoops L, Delahaye L, Kersten MJ, Kibbelaar RE, Wessels LA, et al. Geneexpression and immunohistochemical study of specific T-cell subsets and accessory cell types in the transformation and prognosis of follicular lymphoma. J Clin Oncol. 2007;25 (4):390-8.
11. de Jong D, Fest T. The microenvironment in follicular lymphoma. Best Pract Res Clin Haematol. 2011;24(2):135-46.
12. de Jong D, Rosenwald A, Chhanabhai M, Gaulard P, Klapper W, Lee A, et al. Immunohistochemical prognostic markers in diffuse large B-cell lymphoma: validation of tissue microarray as a prerequisite for broad clinical applications--a study from the Lunenburg Lymphoma Biomarker Consortium. J Clin Oncol. 2007;25(7):805-12.
13. Perez EA, Suman VJ, Davidson NE, Martino S, Kaufman PA, Lingle WL, et al. HER2 testing by local, central, and reference laboratories in specimens from the North Central Cancer Treatment Group N9831 intergroup adjuvant trial. J Clin Oncol. 2006;24(19): 3032-8.
14. Ruschoff J, Kerr KM, Grote HJ, Middel P, von Heydebreck A, Alves VA, et al. Reproducibility of Immunohistochemical Scoring for Epidermal Growth Factor Receptor Expression in Non-Small Cell Lung Cancer. Arch Pathol Lab Med. 2013;137(9): 1255-61.
15. Farinha P, Masoudi H, Skinnider BF, Shumansky K, Spinelli JJ, Gill K, et al. Analysis of multiple biomarkers shows that lymphoma-associated macrophage (LAM) content is an independent predictor of survival in follicular lymphoma (FL). Blood. 2005;106(6):2169-74.
16. de Jong D, Koster A, Hagenbeek A, Raemaekers J, Veldhuizen D, Heisterkamp S, et al. Impact of the tumor microenvironment on prognosis in follicular lymphoma is dependent on specific treatment protocols. Haematologica. 2009;94(1):70-7.
17. Carreras J, Lopez-Guillermo A, Roncador G, Villamor N, Colomo L, Martinez A, et al. High numbers of tumor-infiltrating programmed cell death 1-positive regulatory lymphocytes are associated with improved overall survival in follicular lymphoma. J Clin Oncol. 2009;27(9):1470-6.
18. Alvaro T, Lejeune M, Salvado MT, Lopez C, Jaen J, Bosch R, et al. Immunohistochemical patterns of reactive microenvironment are associated with clinicobiologic behavior in follicular lymphoma patients. J Clin Oncol. 2006;24(34):5350-7.
19. Carreras J, Lopez-Guillermo A, Fox BC, Colomo L, Martinez A, Roncador G, et al. High numbers of tumor-infiltrating FOXP3-positive regulatory T cells are associated with improved overall survival in follicular lymphoma. Blood. 2006;108(9):2957-64.
20. Wahlin BE, Aggarwal M, Montes-Moreno S, Gonzalez LF, Roncador G, Sanchez-Verde L, et al. A unifying microenvironment model in follicular lymphoma: outcome is predicted by programmed death-1--positive, regulatory, cytotoxic, and helper T cells and macrophages. Clin Cancer Res. 2010;16(2): 637-50.
21. Wahlin BE, Sundstrom C, Holte H, Hagberg H, Erlanson M, Nilsson-Ehle H, et al. T cells in tumors and blood predict outcome in follicular lymphoma treated with rituximab. Clin Cancer Res. 2011;17(12):4136-44.
22. Farinha P, Al-Tourah A, Gill K, Klasa R, Connors JM, Gascoyne RD. The architectural pattern of FOXP3-positive T cells in follicular lymphoma is an independent predictor of survival and histologic transformation. Blood. 2010;115(2):289-95.
23. Lee AM, Clear AJ, Calaminici M, Davies AJ, Jordan S, MacDougall F, et al. Number of CD4+ cells and location of forkhead box protein P3-positive cells in diagnostic follicular lymphoma tissue microarrays correlates with outcome. J Clin Oncol. 2006;24(31): 5052-9.
24. Carbone A, Gloghini A, Gruss HJ, Pinto A. CD40 ligand is constitutively expressed in a subset of T cell lymphomas and on the microenvironmental reactive T cells of follicular lymphomas and Hodgkin's disease. Am J Pathol. 1995;147(4):912-22.
25. Ghia P, Boussiotis VA, Schultze JL, Cardoso AA, Dorfman DM, Gribben JG, et al. Unbalanced expression of bcl-2 family proteins in follicular lymphoma: contribution of CD40 signaling in promoting survival. Blood. 1998;91(1):244-51.
26. Buske C, Twiling A, Gogowski G, Schreiber K, Feuring-Buske M, Wulf GG, et al. In vitro activation of low-grade non-Hodgkin's lymphoma by murine fibroblasts, IL-4, anti-CD40 antibodies and the soluble CD40 ligand. Leukemia 1997;11(11):1862-7.
27. Irish JM, Myklebust JH, Alizadeh AA, Houot R, Sharman JP, Czerwinski DK, et al. B-cell signaling networks reveal a negative prognostic human lymphoma cell subset that emerges during tumor progression. Proc Natl Acad Sci USA. 2010; 107(29):12747-54.
28. Epron G, Ame-Thomas P, Le Priol J, Pangault C, Dulong J, Lamy T, et al. Monocytes and T cells cooperate to favor normal and follicular lymphoma B-cell growth: role of IL-15 and CD40L signaling. Leukemia 2012;26(1):139-48.
29. Johnson PW, Watt SM, Betts DR, Davies D, Jordan S, Norton AJ, et al. Isolated follicular lymphoma cells are resistant to apoptosis and can be grown in vitro in the CD40/stromal cell system. Blood. 1993;82(6):1848-57.
30. Schmitter D, Koss M, Niederer E, Stahel RA, Pichert G. T-cell derived cytokines co-stimulate proliferation of CD40-activated germinal centre as well as follicular lymphoma cells. Hematol Oncol. 1997;15(4):197-207.
31. Travert M, Ame-Thomas P, Pangault C, Morizot A, Micheau O, Semana G, et al. CD40 ligand protects from TRAIL-induced apoptosis in follicular lymphomas through NF-kappaB activation and up-regulation of c-FLIP and Bcl-xL. J Immunol. 2008;181(2): 1001-11.
32. Bohen SP, Troyanskaya OG, Alter O, Warnke R, Botstein D, Brown PO, et al. Variation in gene expression patterns in follicular lymphoma and the response to rituximab. Proc Natl Acad Sci USA. 2003; 100(4):1926-30.
33. Kelley T, Beck R, Absi A, Jin T, Pohlman B, Hsi E. Biologic predictors in follicular lymphoma: importance of markers of immune response. Leuk Lymphoma. 2007;48(12): 2403-11.
34. Wahlin BE, Sander B, Christensson B, Kimby E. CD8+ T-cell content in diagnostic lymph nodes measured by flow cytometry is a predictor of survival in follicular lymphoma. Clin Cancer Res. 2007;13(2 Pt 1):388-97.
35. Sweetenham JW, Goldman B, LeBlanc ML, Cook JR, Tubbs RR, Press OW, et al. Prognostic value of regulatory T cells, lymphoma-associated macrophages, and MUM-1 expression in follicular lymphoma treated before and after the introduction of monoclonal antibody therapy: a Southwest Oncology Group Study. Ann Oncol. 2010; 21(6):1196-202.
36. Klapper W, Hoster E, Rolver L, Schrader C, Janssen D, Tiemann M, et al. Tumor sclerosis but not cell proliferation or malignancy grade is a prognostic marker in advancedstage follicular lymphoma: the German Low Grade Lymphoma Study Group. J Clin Oncol. 2007;25(22):3330-6.
37. Taskinen M, Karjalainen-Lindsberg ML, Leppa S. Prognostic influence of tumor-infiltrating mast cells in patients with follicular lymphoma treated with rituximab and CHOP. Blood. 2008;111(9):4664-7.
38. Taskinen M, Karjalainen-Lindsberg ML, Nyman H, Eerola LM, Leppa S. A high tumor-associated macrophage content predicts favorable outcome in follicular lymphoma patients treated with rituximab and cyclophosphamide-doxorubicin-vincristineprednisone. Clin Cancer Res. 2007;13(19): 5784-9.
39. Alvaro T, Lejeune M, Camacho FI, Salvado MT, Sanchez L, Garcia JF, et al. The presence of STAT1-positive tumor-associated macrophages and their relation to outcome in patients with follicular lymphoma. Haematologica. 2006;91(12):1605-12.
40. Farinha P, Kyle AH, Minchinton AI, Connors JM, Karsan A, Gascoyne RD. Vascularization predicts overall survival and risk of transformation in follicular lymphoma. Haematologica. 2010;95(12):2157-60.
41. Taskinen M, Jantunen E, Kosma VM, Bono P, Karjalainen-Lindsberg ML, Leppa S. Prognostic impact of CD31-positive microvessel density in follicular lymphoma patients treated with immunochemotherapy. Eur J Cancer. 2010;46(13):2506-12.
42. Clear AJ, Lee AM, Calaminici M, Ramsay AG, Morris KJ, Hallam S, et al. Increased angiogenic sprouting in poor prognosis FL is associated with elevated numbers of CD163+ macrophages within the immediate sprouting microenvironment. Blood. 2010;115(24):5053-6.
43. Leich E, Ott G, Rosenwald A. Pathology, pathogenesis and molecular genetics of follicular NHL. Best Pract Res Clin Haematol. 2011;24(2):95-109.
44. Craig FE, Foon KA. Flow cytometric immunophenotyping for hematologic neoplasms. Blood. 2008;111(8):3941-67.