Evaluation of Immunophenotypic and Molecular Biomarkers for Sézary Syndrome Using Standard Operating Procedures: A Multicenter Study of 59 Patients

Journal of Investigative Dermatology

Volumn 136, Issue 7, 2016, Pages 1364-1372

  Boonk, Stephanie E ^a   Zoutman, Willem H ^a   Marie Cardine, Anne ^b,c   van der Fits, Leslie ^a   Out Luiting, Jacoba J ^a   Mitchell, Tracey J ^d   Tosi, Isabella ^d   Morris, Stephen L ^e   Moriarty, Blaithin ^d   Booken, Nina ^f   Felcht, Moritz ^f   Quaglino, Pietro ^g   Ponti, Renata ^g   Barberio, Emanuela ^g   Ram Wolff, Caroline ^b,c   Jäntti, Kirsi ^h   Ranki, Annamari ^h   Bernengo, Maria Grazia ^g   Klemke, Claus Detlev ^f   Bensussan, Armand ^b,c   Michel, Laurence ^b,c   Whittaker, Sean ^d   Bagot, Martine ^b,c   Tensen, Cornelis P ^a   Willemze, Rein ^a   Vermeer, Maarten H ^a   more..

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b SAINT LOUIS HOSPITAL   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d ST THOMAS HOSPITAL   (United Kingdom)

^e GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

^f UNIVERSITY OF HEIDELBERG   (Germany)

^g UNIVERSITY OF TURIN   (Italy)

^h HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CD1D ANTIGEN; CD7 ANTIGEN; CDO1 PROTEIN; CELL SURFACE PROTEIN; DIPEPTIDYL PEPTIDASE IV; DNM3 PROTEIN; EPHRIN RECEPTOR A4; MNT PROTEIN; MYC PROTEIN; PLS3 PROTEIN; PROTEIN; STAT4 PROTEIN; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR JUNB; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TWIST1 PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; COPY NUMBER VARIATION; DIAGNOSTIC TEST ACCURACY STUDY; DOWN REGULATION; EUROPE; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; IMMUNOPHENOTYPING; MAJOR CLINICAL STUDY; MALE; MULTICENTER STUDY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; SEZARY SYNDROME; UPREGULATION; CLINICAL TRIAL; CYTOLOGY; DIFFERENTIAL DIAGNOSIS; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNOLOGY; INFLAMMATION; MIDDLE AGED; REPRODUCIBILITY; SKIN DISEASES; STANDARDS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BIOMARKERS; CD4-POSITIVE T-LYMPHOCYTES; DIAGNOSIS, DIFFERENTIAL; EUROPE; FEMALE; FLOW CYTOMETRY; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; IMMUNOPHENOTYPING; INFLAMMATION; MALE; MIDDLE AGED; POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SEZARY SYNDROME; SKIN DISEASES;

EID: 84992504078     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1016/j.jid.2016.01.038     Document Type: Article

References (45)

1. Bagot, M., Moretta, A., Sivori, S., Biassoni, R., Cantoni, C., Bottino, C., et al. CD4(+) cutaneous T-cell lymphoma cells express the p140-killer cell immunoglobulin-like receptor. Blood 97 (2001), 1388–1391.
2. Bahler, D.W., Hartung, L., Hill, S., Bowen, G.M., Vonderheid, E.C., CD158k/KIR3DL2 is a useful marker for identifying neoplastic T-cells in Sezary syndrome by flow cytometry. Cytometry B Clin Cytom 74 (2008), 156–162.
3. Bernengo, M.G., Novelli, M., Quaglino, P., Lisa, F., De Matteis, A., Savoia, P., et al. The relevance of the CD4+ CD26- subset in the identification of circulating Sézary cells. Br J Dermatol 144 (2001), 125–135.
4. Booken, N., Gratchev, A., Utikal, J., Weiss, C., Yu, X., Qadoumi, M., et al. Sezary syndrome is a unique cutaneous T-cell lymphoma as identified by an expanded gene signature including diagnostic marker molecules CDO1 and DNM3. Leukemia 22 (2008), 393–399.
5. Campbell, J.J., Clark, R.A., Watanabe, R., Kupper, T.S., Sezary syndrome and mycosis fungoides arise from distinct T-cell subsets: a biologic rationale for their distinct clinical behaviors. Blood 116 (2010), 767–771.
6. Dummer, R., Heald, P.W., Nestle, F.O., Ludwig, E., Laine, E., Hemmi, S., et al. Sezary syndrome T-cell clones display T-helper 2 cytokines and express the accessory factor-1 (interferon-gamma receptor beta-chain). Blood 88 (1996), 1383–1389.
7. Duncan, S.C., Winkelmann, R.K., Circulating Sézary cells in hospitalized dermatology patients. Br J Dermatol 99 (1978), 171–178.
8. Fierro, M.T., Novelli, M., Quaglino, P., Comessatti, A., Fava, P., Ortoncelli, M., et al. Heterogeneity of circulating CD4+ memory T-cell subsets in erythrodermic patients: CD27 analysis can help to distinguish cutaneous T-cell lymphomas from inflammatory erythroderma. Dermatology 216 (2008), 213–221.
9. Goswami, M., Duvic, M., Dougherty, A., Ni, X., Increased Twist expression in advanced stage of mycosis fungoides and Sezary syndrome. J Cutan Pathol 39 (2012), 500–507.
10. Harmon, C.B., Witzig, T.E., Katzmann, J.A., Pittelkow, M.R., Detection of circulating T cells with CD4+CD7- immunophenotype in patients with benign and malignant lymphoproliferative dermatoses. J Am Acad Dermatol 35 (1996), 404–410.
11. Jones, D., Dang, N.H., Duvic, M., Washington, L.T., Huh, Y.O., Absence of CD26 expression is a useful marker for diagnosis of T-cell lymphoma in peripheral blood. Am J Clin Pathol 115 (2001), 885–892.
12. Karenko, L., Nevala, H., Raatikainen, M., Franssila, K., Ranki, A., Chromosomally clonal T cells in the skin, blood, or lymph nodes of two Sezary syndrome patients express CD45RA, CD45RO, CDw150, and interleukin-4, but no interleukin-2 or interferon-gamma. J Invest Dermatol 116 (2001), 188–193.
13. Kari, L., Loboda, A., Nebozhyn, M., Rook, A.H., Vonderheid, E.C., Nichols, C., et al. Classification and prediction of survival in patients with the leukemic phase of cutaneous T cell lymphoma. J Exp Med 197 (2003), 1477–1488.
14. Kelemen, K., Guitart, J., Kuzel, T.M., Goolsby, C.L., Peterson, L.C., The usefulness of CD26 in flow cytometric analysis of peripheral blood in Sezary syndrome. Am J Clin Pathol 129 (2008), 146–156.
15. Klemke, C.D., Brade, J., Weckesser, S., Sachse, M.M., Booken, N., Neumaier, M., et al. The diagnosis of Sezary syndrome on peripheral blood by flow cytometry requires the use of multiple markers. Br J Dermatol 159 (2008), 871–880.
16. Lima, M., Almeida, J., dos Anjos, T.M., Queiros, M.L., Santos, A.H., Fonseca, S., et al. Utility of flow cytometry immunophenotyping and DNA ploidy studies for diagnosis and characterization of blood involvement in CD4+ Sezary's syndrome. Haematologica 88 (2003), 874–887.
17. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001), 402–408.
18. Mao, X., Orchard, G., Lillington, D.M., Russell-Jones, R., Young, B.D., Whittaker, S.J., Amplification and overexpression of JUNB is associated with primary cutaneous T-cell lymphomas. Blood 101 (2003), 1513–1519.
19. Mao, X., Orchard, G., Mitchell, T.J., Oyama, N., Russell-Jones, R., Vermeer, M.H., et al. A genomic and expression study of AP-1 in primary cutaneous T-cell lymphoma: evidence for dysregulated expression of JUNB and JUND in MF and SS. J Cutan Pathol 35 (2008), 899–910.
20. Marie-Cardine, A., Huet, D., Ortonne, N., Remtoula, N., Le, G.S., Bagot, M., et al. Killer cell Ig-like receptors CD158a and CD158b display a coactivatory function, involving the c-Jun NH2-terminal protein kinase signaling pathway, when expressed on malignant CD4+ T cells from a patient with Sezary syndrome. Blood 109 (2007), 5064–5065.
21. Meijer, C.J., van Leeuwen, A.W., van der Loo, E.M., van de Putte, L.B., van Vloten, W.A., Cerebriform (Sezary like) mononuclear cells in healthy individuals: a morphologically distinct population of T cells. Relationship with mycosis fungoides and Sezary's syndrome. Virchows Arch B Cell Pathol 25 (1977), 95–104.
22. Michel, L., Jean-Louis, F., Begue, E., Bensussan, A., Bagot, M., Use of PLS3, Twist, CD158k/KIR3DL2, and NKp46 gene expression combination for reliable Sezary syndrome diagnosis. Blood 121 (2013), 1477–1478.
23. Moins-Teisserenc, H., Daubord, M., Clave, E., Douay, C., Felix, J., Marie-Cardine, A., et al. CD158k is a reliable marker for diagnosis of Sezary syndrome and reveals an unprecedented heterogeneity of circulating malignant cells. J Invest Dermatol 135 (2015), 247–257.
24. Nagler, A.R., Samimi, S., Schaffer, A., Vittorio, C.C., Kim, E.J., Rook, A.H., Peripheral blood findings in erythrodermic patients: importance for the differential diagnosis of Sezary syndrome. J Am Acad Dermatol 66 (2012), 503–508.
25. Nebozhyn, M., Loboda, A., Kari, L., Rook, A.H., Vonderheid, E.C., Lessin, S., et al. Quantitative PCR on 5 genes reliably identifies CTCL patients with 5% to 99% circulating tumor cells with 90% accuracy. Blood 107 (2006), 3189–3196.
26. Olsen, E., Vonderheid, E., Pimpinelli, N., Willemze, R., Kim, Y., Knobler, R., et al. Revisions to the staging and classification of mycosis fungoides and Sezary syndrome: a proposal of the International Society for Cutaneous Lymphomas (ISCL) and the cutaneous lymphoma task force of the European Organization of Research and Treatment of Cancer (EORTC). Blood 110 (2007), 1713–1722.
27. Poszepczynska-Guigne, E., Schiavon, V., d'Incan, M., Echchakir, H., Musette, P., Ortonne, N., et al. CD158k/KIR3DL2 is a new phenotypic marker of Sezary cells: relevance for the diagnosis and follow-up of Sezary syndrome. J Invest Dermatol 122 (2004), 820–823.
28. Rappl, G., Muche, J.M., Abken, H., Sterry, W., Tilgen, W., Ugurel, S., et al. CD4(+)CD7(-) T cells compose the dominant T-cell clone in the peripheral blood of patients with Sezary syndrome. J Am Acad Dermatol 44 (2001), 456–461.
29. Sentis, H.J., Willemze, R., Scheffer, E., Histopathologic studies in Sezary syndrome and erythrodermic mycosis fungoides: a comparison with benign forms of erythroderma. J Am Acad Dermatol 15 (1986), 1217–1226.
30. Sokolowska-Wojdylo, M., Wenzel, J., Gaffal, E., Steitz, J., Roszkiewicz, J., Bieber, T., et al. Absence of CD26 expression on skin-homing CLA+ CD4+ T lymphocytes in peripheral blood is a highly sensitive marker for early diagnosis and therapeutic monitoring of patients with Sezary syndrome. Clin Exp Dermatol 30 (2005), 702–706.
31. Su, M.W., Dorocicz, I., Dragowska, W.H., Ho, V., Li, G., Voss, N., et al. Aberrant expression of T-plastin in Sezary cells. Cancer Res 63 (2003), 7122–7127.
32. Swerdlow, S.H., Campo, E., Lee Harris, N., Jaffe, E.S., Pileri, S.A., Stein, H., et al. WHO classification of tumours of haematopoietic and lymphoid tissues. 2008, WHO Press, Geneva, Switzerland, 299.
33. Trotter, M.J., Whittaker, S.J., Orchard, G.E., Smith, N.P., Cutaneous histopathology of Sezary syndrome: a study of 41 cases with a proven circulating T-cell clone. J Cutan Pathol 24 (1997), 286–291.
34. Van Dongen, J.J., Orfao, A., EuroFlow Consortium: EuroFlow. Resetting leukemia and lymphoma immunophenotyping. Basis for companion diagnostics and personalized medicine. Leukemia 26 (2012), 1899–1907.
35. Van Doorn, R., Dijkman, R., Vermeer, M.H., Out-Luiting, J.J., van der Raaij-Helmer, E.M., Willemze, R., et al. Aberrant expression of the tyrosine kinase receptor EphA4 and the transcription factor twist in Sezary syndrome identified by gene expression analysis. Cancer Res 64 (2004), 5578–5586.
36. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology, 3, 2002.
37. Vermeer, M.H., van Doorn, R., Dijkman, R., Mao, X., Whittaker, S., van Voorst Vader, P.C., et al. Novel and highly recurrent chromosomal alterations in Sezary syndrome. Cancer Res 68 (2008), 2689–2698.
38. Vonderheid, E.C., On the diagnosis of erythrodermic cutaneous T-cell lymphoma. J Cutan Pathol 1:Suppl. 33 (2006), 27–42.
39. Vonderheid, E.C., Bernengo, M.G., The Sezary syndrome: hematologic criteria. Hematol Oncol Clin North Am 17 (2003), 1367–1389.
40. Vonderheid, E.C., Bernengo, M.G., Burg, G., Duvic, M., Heald, P., Laroche, L., et al. Update on erythrodermic cutaneous T-cell lymphoma: report of the International Society for Cutaneous Lymphomas. J Am Acad Dermatol 46 (2002), 95–106.
41. Washington, L.T., Huh, Y.O., Powers, L.C., Duvic, M., Jones, D., A stable aberrant immunophenotype characterizes nearly all cases of cutaneous T-cell lymphoma in blood and can be used to monitor response to therapy. BMC Clin Pathol, 2, 2002, 5.
42. Westers, T.M., Ireland, R., Kern, W., Alhan, C., Balleisen, J.S., Bettelheim, P., et al. Standardization of flow cytometry in myelodysplastic syndromes: a report from an international consortium and the European LeukemiaNet Working Group. Leukemia 26 (2012), 1730–1741.
43. Wieselthier, J.S., Koh, H.K., Sezary syndrome: diagnosis, prognosis, and critical review of treatment options. J Am Acad Dermatol 22 (1990), 381–401.
44. Willemze, R., Kerl, H., Sterry, W., Berti, E., Cerroni, L., Chimenti, S., et al. EORTC classification for primary cutaneous lymphomas: a proposal from the Cutaneous Lymphoma Study Group of the European Organization for Research and Treatment of Cancer. Blood 90 (1997), 354–371.
45. Willemze, R., Jaffe, E.S., Burg, G., Cerroni, L., Berti, E., Swerdlow, S.H., et al. WHO-EORTC classification for cutaneous lymphomas. Blood 105 (2005), 3768–3785.