Primary cutaneous T-cell lymphoma (mycosis fungoides and Sézary syndrome): Part I. Diagnosis: Clinical and histopathologic features and new molecular and biologic markers

Journal of the American Academy of Dermatology

Volumn 70, Issue 2, 2014, Pages 205.e1-205.e16

  Jawed, Sarah I ^a   Myskowski, Patricia L ^a   Horwitz, Steven ^a   Moskowitz, Alison ^a   Querfeld, Christiane ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

biologic and molecular markers; clinical and diagnostic challenges; cutaneous T cell lymphoma; genetic aberrations; histopathology; mycosis fungoides; mycosis fungoides subtypes; pathogenesis; prognostic value; S zary syndrome; skin homing features; transformed mycosis fungoides; tumor microenvironment

Indexed keywords

BIOLOGICAL MARKER; CELL ADHESION MOLECULE; PROGRAMMED DEATH 1 RECEPTOR; T LYMPHOCYTE RECEPTOR;

APOPTOSIS; ARTICLE; CANCER GROWTH; CD4+ T LYMPHOCYTE; CELL HOMING; CHROMOSOME ABERRATION; CLASSIC MYCOSIS FUNGOIDES; CLINICAL FEATURE; CLONAL VARIATION; CUTANEOUS T CELL LYMPHOMA; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DISEASE CLASSIFICATION; ERYTHRODERMIC MYCOSIS FUNGOIDES; FOLLICULOTROPIC MYCOSIS FUNGOIDES; GENE REARRANGEMENT; GRANULOMATOUS MYCOSIS FUNGOIDES; GRANULOMATOUS SLACK SKIN; HISTOPATHOLOGY; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOPHENOTYPING; MEMORY T LYMPHOCYTE; MORBIDITY; MYCOSIS FUNGOIDES; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SEZARY SYNDROME; SKIN DEFECT; SURVIVAL RATE; T LYMPHOCYTE RECEPTOR GENE; TUMOR MICROENVIRONMENT; WORINGER KOLOPP DISEASE; CD4 LYMPHOCYTE COUNT; DIFFERENTIAL DIAGNOSIS; FEMALE; IMMUNOLOGY; LYMPHOMA, T-CELL, CUTANEOUS; MALE; MEDICAL EDUCATION; NEEDLE BIOPSY; PATHOLOGY; PATHOPHYSIOLOGY; SENSITIVITY AND SPECIFICITY; SKIN NEOPLASMS;

BIOLOGICAL MARKERS; BIOPSY, NEEDLE; CD4 LYMPHOCYTE COUNT; DIAGNOSIS, DIFFERENTIAL; EDUCATION, MEDICAL, CONTINUING; FEMALE; HUMANS; LYMPHOMA, T-CELL, CUTANEOUS; MALE; MYCOSIS FUNGOIDES; SENSITIVITY AND SPECIFICITY; SEZARY SYNDROME; SKIN NEOPLASMS;

EID: 84892647296     PISSN: 01909622     EISSN: 10976787     Source Type: Journal    
DOI: 10.1016/j.jaad.2013.07.049     Document Type: Review

References (133)

1. R. Willemze, E.S. Jaffe, G. Burg, L. Cerroni, E. Berti, and S.H. Swerdlow et al. WHO-EORTC classification for cutaneous lymphomas Blood 105 2005 3768 3785
2. G.P. Sarantopoulos, B. Palla, J. Said, M.C. Kinney, S.M. Swerdlow, and R. Willemze et al. Mimics of cutaneous lymphoma: report of the 2011 Society for Hematopathology/European Association for Haematopathology workshop Am J Clin Pathol 139 2013 536 551
3. H.S. Zackheim, and T.H. McCalmont Mycosis fungoides: the great imitator J Am Acad Dermatol 47 2002 914 918
4. P.T. Bradford, S.S. Devesa, W.F. Anderson, and J.R. Toro Cutaneous lymphoma incidence patterns in the United States: a population-based study of 3884 cases Blood 113 2009 5064 5073
5. V.D. Criscione, and M.A. Weinstock Incidence of cutaneous T-cell lymphoma in the United States, 1973-2002 Arch Dermatol 143 2007 854 859
6. J.J. Crowley, A. Nikko, A. Varghese, R.T. Hoppe, and Y.H. Kim Mycosis fungoides in young patients: clinical characteristics and outcome J Am Acad Dermatol 38 1998 696 701
7. E. Pope, S. Weitzman, B. Ngan, S. Walsh, K. Morel, and J. Williams et al. Mycosis fungoides in the pediatric population: report from an international Childhood Registry of Cutaneous Lymphoma J Cutan Med Surg 14 2010 1 6
8. K.P. Huang, M.A. Weinstock, C.A. Clarke, A. McMillan, R.T. Hoppe, and Y.H. Kim Second lymphomas and other malignant neoplasms in patients with mycosis fungoides and Sézary syndrome: evidence from population-based and clinical cohorts Arch Dermatol 143 2007 45 50
9. M. Girardi, P.W. Heald, and L.D. Wilson The pathogenesis of mycosis fungoides N Engl J Med 350 2004 1978 1988
10. B. Pigozzi, and M. Bordignon Belloni Fortina A, Michelotto G, Alaibac M. Expression of the CD1a molecule in B- and T-lymphoproliferative skin conditions Oncol Rep 15 2006 347 351
11. M. Storz, K. Zepter, J. Kamarashev, R. Dummer, G. Burg, and A.C. Haffner Coexpression of CD40 and CD40 ligand in cutaneous T-cell lymphoma (mycosis fungoides) Cancer Res 61 2001 452 454
12. B.J. Nickoloff, F.O. Nestle, X.G. Zheng, and L.A. Turka T lymphocytes in skin lesions of psoriasis and mycosis fungoides express B7-1: a ligand for CD28 Blood 83 1994 2580 2586
13. C.M. Jackow, J.B. McHam, A. Friss, J. Alvear, J.R. Reveille, and M. Duvic HLA-DR5 and DQB1*03 class II alleles are associated with cutaneous T-cell lymphoma J Invest Dermatol 107 1996 373 376
14. V. Jarrousse, G. Quereux, S. Marques-Briand, A.C. Knol, A. Khammari, and B. Dreno Toll-like receptors 2, 4 and 9 expression in cutaneous T-cell lymphoma (mycosis fungoides and Sézary syndrome) Eur J Dermatol 16 2006 636 641
15. A.T. Ermertcan, F. Ozturk, and K. Gunduz Toll-like receptors and skin J Eur Acad Dermatol Venereol 25 2011 997 1006
16. Z. Khamaysi, S. Weltfriend, K. Khamaysi, and R. Bergman Contact hypersensitivity in patients with primary cutaneous lymphoproliferative disorders Int J Dermatol 50 2011 423 427
17. J.G. Orbaneja, L.I. Diez, J.L. Lozano, and L.C. Salazar Lymphomatoid contact dermatitis: a syndrome produced by epicutaneous hypersensitivity with clinical features and a histopathologic picture similar to that of mycosis fungoides Contact Dermatitis 2 1976 139 143
18. R. Talpur, R. Bassett, and M. Duvic Prevalence and treatment of Staphylococcus aureus colonization in patients with mycosis fungoides and Sézary syndrome Br J Dermatol 159 2008 105 112
19. G.S. Wood, J.M. Schaffer, R. Boni, R. Dummer, G. Burg, and M. Takeshita et al. No evidence of HTLV-I proviral integration in lymphoproliferative disorders associated with cutaneous T-cell lymphoma Am J Pathol 150 1997 667 673
20. B.A. Pancake, D. Zucker-Franklin, and E.E. Coutavas The cutaneous T cell lymphoma, mycosis fungoides, is a human T cell lymphotropic virus-associated disease. A study of 50 patients J Clin Invest 95 1995 547 554
21. D. Zucker-Franklin, and B.A. Pancake The role of human T-cell lymphotropic viruses (HTLV-I and II) in cutaneous T-cell lymphomas Semin Dermatol 13 1994 160 165
22. K.L. Herne, R. Talpur, J. Breuer-McHam, R. Champlin, and M. Duvic Cytomegalovirus seropositivity is significantly associated with mycosis fungoides and Sézary syndrome Blood 101 2003 2132 2136
23. Y. Rodriguez-Gil, S.I. Palencia, F. Lopez-Rios, P.L. Ortiz, and J.L. Rodriguez-Peralto Mycosis fungoides after solid-organ transplantation: report of 2 new cases Am J Dermatopathol 30 2008 150 155
24. F.E. Ravat, M.F. Spittle, and R. Russell-Jones Primary cutaneous T-cell lymphoma occurring after organ transplantation J Am Acad Dermatol 54 2006 668 675
25. D.M. McMullan, B. Radovaneevic, C.M. Jackow, O.H. Frazier, and M. Duvic Cutaneous T-cell lymphoma in a cardiac transplant recipient Tex Heart Inst J 28 2001 203 207
26. M.K. Burns, and K.D. Cooper Cutaneous T-cell lymphoma associated with HIV infection J Am Acad Dermatol 29 1993 394 399
27. J. Guitart HIV-1 and an HTLV-II-associated cutaneous T-cell lymphoma N Engl J Med 343 2000 303 304
28. M.H. Greene, N.A. Dalager, S.I. Lamberg, C.E. Argyropoulos, and J.F. Fraumeni Jr. Mycosis fungoides: epidemiologic observations Cancer Treat Rep 63 1979 597 606
29. M.M. Morales-Suárez-Varela, J. Olsen, P. Johansen, L. Kaerlev, P. Guénel, and P. Arveux et al. Occupational risk factors for mycosis fungoides: a European multicenter case-control study J Occup Environ Med 46 2004 205 211
30. J.H. Cho-Vega, J.A. Tschen, M. Duvic, and F. Vega Early-stage mycosis fungoides variants: case-based review Ann Diagn Pathol 14 2010 369 385
31. Y.H. Kim, H.L. Liu, S. Mraz-Gernhard, A. Varghese, and R.T. Hoppe Long-term outcome of 525 patients with mycosis fungoides and Sézary syndrome: clinical prognostic factors and risk for disease progression Arch Dermatol 139 2003 857 866
32. E.C. Vonderheid, M.G. Bernengo, G. Burg, M. Duvic, P. Heald, and L. Laroche 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
33. E. Olsen, E. Vonderheid, N. Pimpinelli, R. Willemze, Y. Kim, and R. Knobler et al. Revisions to the staging and classification of mycosis fungoides and Sézary 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
34. H. Diwan, and D. Ivan CD8-positive mycosis fungoides and primary cutaneous aggressive epidermotropic CD8-positive cytotoxic T-cell lymphoma J Cutan Pathol 36 2009 390 392
35. + cytotoxic variant of mycosis fungoides: a case series of seven patients Br J Dermatol 161 2009 826 830
36. G. Burg, W. Kempf, A. Cozzio, J. Feit, R. Willemze, and E.S. Jaffe et al. WHO/EORTC classification of cutaneous lymphomas 2005: histological and molecular aspects J Cutan Pathol 32 2005 647 674
37. B.R. Smoller, K. Bishop, E. Glusac, Y.H. Kim, and M. Hendrickson Reassessment of histologic parameters in the diagnosis of mycosis fungoides Am J Surg Pathol 19 1995 1423 1430
38. J.L. Sanchez, and A.B. Ackerman The patch stage of mycosis fungoides. Criteria for histologic diagnosis Am J Dermatopathol 1 1979 5 26
39. N. Pimpinelli, E.A. Olsen, M. Santucci, E. Vonderheid, A.C. Haeffner, and S. Stevens et al. Defining early mycosis fungoides J Am Acad Dermatol 53 2005 1053 1063
40. M. Santucci, A. Biggeri, A.C. Feller, and G. Burg Accuracy, concordance, and reproducibility of histologic diagnosis in cutaneous T-cell lymphoma: an EORTC Cutaneous Lymphoma Project Group Study. European Organization for Research and Treatment of Cancer Arch Dermatol 136 2000 497 502
41. M. Santucci, A. Biggeri, A.C. Feller, D. Massi, and G. Burg Efficacy of histologic criteria for diagnosing early mycosis fungoides: an EORTC cutaneous lymphoma study group investigation. European Organization for Research and Treatment of Cancer Am J Surg Pathol 24 2000 40 50
42. P.E. Shapiro, and F.J. Pinto The histologic spectrum of mycosis fungoides/Sézary syndrome (cutaneous T-cell lymphoma). A review of 222 biopsies, including newly described patterns and the earliest pathologic changes Am J Surg Pathol 18 1994 645 667
43. Z.S. Naraghi, H. Seirafi, M. Valikhani, F. Farnaghi, S. Kavusi, and Y. Dowlati Assessment of histologic criteria in the diagnosis of mycosis fungoides Int J Dermatol 42 2003 45 52
44. C. Massone, K. Kodama, H. Kerl, and L. Cerroni Histopathologic features of early (patch) lesions of mycosis fungoides: a morphologic study on 745 biopsy specimens from 427 patients Am J Surg Pathol 29 2005 550 560
45. J. Guitart, J. Kennedy, S. Ronan, J.S. Chmiel, Y.C. Hsiegh, and D. Variakojis Histologic criteria for the diagnosis of mycosis fungoides: proposal for a grading system to standardize pathology reporting J Cutan Pathol 28 2001 174 183
46. S. Kohler, Y.H. Kim, and B.R. Smoller Histologic criteria for the diagnosis of erythrodermic mycosis fungoides and Sézary syndrome: a critical reappraisal J Cutan Pathol 24 1997 292 297
47. N.M. Walsh, R. Prokopetz, V.A. Tron, D.M. Sawyer, A.K. Watters, and S. Murray et al. Histopathology in erythroderma: review of a series of cases by multiple observers J Cutan Pathol 21 1994 419 423
48. K. Nasu, J. Said, E. Vonderheid, J. Olerud, D. Sako, and M. Kadin Immunopathology of cutaneous T-cell lymphomas Am J Pathol 119 1985 436 447
49. E. Ralfkiaer, T.A. Saati, J. Bosq, G. Delsol, K.C. Gatter, and D.Y. Mason Immunocytochemical characterisation of cutaneous lymphomas other than mycosis fungoides J Clin Pathol 39 1986 553 563
50. R. Willemze, C.B. de Graaff-Reitsma, J. Cnossen, W.A. Van Vloten, and C.J. Meijer Characterization of T-cell subpopulations in skin and peripheral blood of patients with cutaneous T-cell lymphomas and benign inflammatory dermatoses J Invest Dermatol 80 1983 60 66
51. C.M. Payne, T.M. Grogan, and P.J. Lynch An ultrastructural morphometric and immunohistochemical analysis of cutaneous lymphomas and benign lymphocytic infiltrates of skin. Useful criteria for diagnosis Arch Dermatol 122 1986 1139 1154
52. B.F. Haynes, L.L. Hensley, and B.V. Jegasothy Phenotypic characterization of skin-infiltrating T cells in cutaneous T-cell lymphoma: comparison with benign cutaneous T-cell infiltrates Blood 60 1982 463 473
53. A. Ormsby, W.F. Bergfeld, R.R. Tubbs, and E.D. Hsi Evaluation of a new paraffin-reactive CD7 T-cell deletion marker and a polymerase chain reaction-based T-cell receptor gene rearrangement assay: implications for diagnosis of mycosis fungoides in community clinical practice J Am Acad Dermatol 45 2001 405 413
54. S.A. Ismail, R. Han, S.L. Sanborn, S.R. Stevens, K.D. Cooper, and G.S. Wood et al. Immunohistochemical staining for CD45R isoforms in paraffin sections to diagnose mycosis fungoides-type cutaneous T-cell lymphoma J Am Acad Dermatol 56 2007 635 642
55. R. Bergman, D. Faclieru, D. Sahar, C.A. Sander, H. Kerner, and Y. Ben-Aryeh et al. Immunophenotyping and T-cell receptor gamma gene rearrangement analysis as an adjunct to the histopathologic diagnosis of mycosis fungoides J Am Acad Dermatol 39 1998 554 559
56. M.L. Lindae, E.A. Abel, R.T. Hoppe, and G.S. Wood Poikilodermatous mycosis fungoides and atrophic large-plaque parapsoriasis exhibit similar abnormalities of T-cell antigen expression Arch Dermatol 124 1988 366 372
57. E. Ralfkiaer, G.L. Wantzin, D.Y. Mason, K. Hou-Jensen, H. Stein, and K. Thomsen Phenotypic characterization of lymphocyte subsets in mycosis fungoides. Comparison with large plaque parapsoriasis and benign chronic dermatoses Am J Clin Pathol 84 1985 610 619
58. G.S. Wood, E.A. Abel, R.T. Hoppe, and R.A. Warnke Leu-8 and Leu-9 antigen phenotypes: immunologic criteria for the distinction of mycosis fungoides from cutaneous inflammation J Am Acad Dermatol 14 1986 1006 1013
59. E.C. Vonderheid, J. Pena, and P. Nowell Sézary cell counts in erythrodermic cutaneous T-cell lymphoma: implications for prognosis and staging Leuk Lymphoma 47 2006 1841 1856
60. - subset in the identification of circulating Sézary cells Br J Dermatol 144 2001 125 135
61. K. Kelemen, C.R. White, K. Gatter, R.M. Braziel, and G. Fan Immunophenotypic correlation between skin biopsy and peripheral blood findings in mycosis fungoides Am J Clin Pathol 134 2010 739 748
62. D. Jones, N.H. Dang, M. Duvic, L.T. Washington, and Y.O. Huh 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
63. N. Ortonne, D. Huet, C. Gaudez, A. Marie-Cardine, V. Schiavon, and M. Bagot et al. Significance of circulating T-cell clones in Sézary syndrome Blood 107 2006 4030 4038
64. C.B. Harmon, T.E. Witzig, J.A. Katzmann, and M.R. Pittelkow 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
65. N. Yawalkar, K. Ferenczi, D.A. Jones, K. Yamanaka, K.Y. Suh, and S. Sadat et al. Profound loss of T-cell receptor repertoire complexity in cutaneous T-cell lymphoma Blood 102 2003 4059 4066
66. G.S. Wood, R.M. Tung, A.C. Haeffner, C.F. Crooks, S. Liao, and R. Orozco et al. Detection of clonal T-cell receptor gamma gene rearrangements in early mycosis fungoides/Sézary syndrome by polymerase chain reaction and denaturing gradient gel electrophoresis (PCR/DGGE) J Invest Dermatol 103 1994 34 41
67. M.H. Delfau-Larue, T. Petrella, C. Lahet, C. Lebozec, M. Bagot, and F. Roudot-Thoraval et al. Value of clonality studies of cutaneous T lymphocytes in the diagnosis and follow-up of patients with mycosis fungoides J Pathol 184 1998 185 190
68. R. Ponti, P. Quaglino, M. Novelli, M.T. Fierro, A. Comessatti, and A. Peroni et al. T-cell receptor gamma gene rearrangement by multiplex polymerase chain reaction/heteroduplex analysis in patients with cutaneous T-cell lymphoma (mycosis fungoides/Sézary syndrome) and benign inflammatory disease: correlation with clinical, histological and immunophenotypical findings Br J Dermatol 153 2005 565 573
69. S.E. Thurber, B. Zhang, Y.H. Kim, I. Schrijver, J. Zehnder, and S. Kohler T-cell clonality analysis in biopsy specimens from two different skin sites shows high specificity in the diagnosis of patients with suggested mycosis fungoides J Am Acad Dermatol 57 2007 782 790
70. S.J. Whittaker, N.P. Smith, R.R. Jones, and L. Luzzatto Analysis of beta, gamma, and delta T-cell receptor genes in mycosis fungoides and Sézary syndrome Cancer 68 1991 1572 1582
71. C. Massone, G. Crisman, H. Kerl, and L. Cerroni The prognosis of early mycosis fungoides is not influenced by phenotype and T-cell clonality Br J Dermatol 159 2008 881 886
72. N.S. Agar, E. Wedgeworth, S. Crichton, T.J. Mitchell, M. Cox, and S. Ferreira et al. Survival outcomes and prognostic factors in mycosis fungoides/Sézary syndrome: validation of the revised International Society for Cutaneous Lymphomas/European Organisation for Research and Treatment of Cancer staging proposal J Clin Oncol 28 2010 4730 4739
73. M.H. Delfau-Larue, S. Dalac, E. Lepage, T. Petrella, J. Wechsler, and J.P. Farcet et al. Prognostic significance of a polymerase chain reaction-detectable dominant T-lymphocyte clone in cutaneous lesions of patients with mycosis fungoides Blood 92 1998 3376 3380
74. P.I. Schiller, M.J. Flaig, U. Puchta, P. Kind, and C.A. Sander Detection of clonal T cells in lichen planus Arch Dermatol Res 292 2000 568 569
75. O. Dereure, E. Levi, and M.E. Kadin T-Cell clonality in pityriasis lichenoides et varioliformis acuta: a heteroduplex analysis of 20 cases Arch Dermatol 136 2000 1483 1486
76. S. Shieh, D.L. Mikkola, and G.S. Wood Differentiation and clonality of lesional lymphocytes in pityriasis lichenoides chronica Arch Dermatol 137 2001 305 308
77. A. Lukowsky, J.M. Muche, W. Sterry, and H. Audring Detection of expanded T cell clones in skin biopsy samples of patients with lichen sclerosus et atrophicus by T cell receptor-gamma polymerase chain reaction assays J Invest Dermatol 115 2000 254 259
78. F. Vega, R. Luthra, L.J. Medeiros, V. Dunmire, S.J. Lee, and M. Duvic et al. Clonal heterogeneity in mycosis fungoides and its relationship to clinical course Blood 100 2002 3369 3373
79. A. Rubben, W. Kempf, M.E. Kadin, D.R. Zimmermann, and G. Burg Multilineage progression of genetically unstable tumor subclones in cutaneous T-cell lymphoma Exp Dermatol 13 2004 472 483
80. + T cells in cutaneous T-cell lymphoma: expression of cytotoxic proteins, Fas ligand, and killing inhibitory receptors and their relationship with clinical behavior J Clin Oncol 19 2001 4322 4329
81. + dendritic cells in mycosis fungoides J Clin Pathol 56 2003 453 458
82. + regulatory T cells in cutaneous T-cell lymphomas: association with disease stage and survival Leukemia 21 2007 2512 2518
83. T. Krejsgaard, N. Odum, C. Geisler, M.A. Wasik, and A. Woetmann Regulatory T cells and immunodeficiency in mycosis fungoides and Sézary syndrome Leukemia 26 2012 424 432
84. + cytotoxic T lymphocytes in mycosis fungoides: a potential mechanism of tumor immune escape? Clin Cancer Res 7 2001 2682 2692
85. C. Gunther, N. Zimmermann, N. Berndt, M. Grosser, A. Stein, and A. Koch et al. Up-regulation of the chemokine CCL18 by macrophages is a potential immunomodulatory pathway in cutaneous T-cell lymphoma Am J Pathol 179 2011 1434 1442
86. M. Sugaya, T. Miyagaki, H. Ohmatsu, H. Suga, H. Kai, and M. Kamata et al. Association of the numbers of CD163(+) cells in lesional skin and serum levels of soluble CD163 with disease progression of cutaneous T cell lymphoma J Dermatol Sci 68 2012 45 51
87. T. Miyagaki, M. Sugaya, H. Suga, H. Ohmatsu, H. Fujita, and Y. Asano et al. Increased CCL18 expression in patients with cutaneous T-cell lymphoma: association with disease severity and prognosis J Eur Acad Dermatol Venereol 27 2013 e60 e67
88. A. Rabenhorst, M. Schlaak, L.C. Heukamp, A. Forster, S. Theurich, and M. von Bergwelt-Baildon et al. Mast cells play a protumorigenic role in primary cutaneous lymphoma Blood 120 2012 2042 2054
89. Y. Reiss, A.E. Proudfoot, C.A. Power, J.J. Campbell, and E.C. Butcher CC chemokine receptor (CCR)4 and the CCR10 ligand cutaneous T cell-attracting chemokine (CTACK) in lymphocyte trafficking to inflamed skin J Exp Med 194 2001 1541 1547
90. K. Ferenczi, R.C. Fuhlbrigge, J. Pinkus, G.S. Pinkus, and T.S. Kupper Increased CCR4 expression in cutaneous T cell lymphoma J Invest Dermatol 119 2002 1405 1410
91. T. Kakinuma, M. Sugaya, K. Nakamura, F. Kaneko, M. Wakugawa, and K. Matsushima et al. Thymus and activation-regulated chemokine (TARC/CCL17) in mycosis fungoides: serum TARC levels reflect the disease activity of mycosis fungoides J Am Acad Dermatol 48 2003 23 30
92. C. Robert, and T.S. Kupper Inflammatory skin diseases, T cells, and immune surveillance N Engl J Med 341 1999 1817 1828
93. H. Yagi, N. Seo, A. Ohshima, T. Itoh, N. Itoh, and T. Horibe et al. Chemokine receptor expression in cutaneous T cell and NK/T-cell lymphomas: immunohistochemical staining and in vitro chemotactic assay Am J Surg Pathol 30 2006 1111 1119
94. T. Yamaguchi, K. Ohshima, T. Tsuchiya, H. Suehuji, K. Karube, and J. Nakayama et al. The comparison of expression of cutaneous lymphocyte-associated antigen (CLA), and Th1- and Th2-associated antigens in mycosis fungoides and cutaneous lesions of adult T-cell leukemia/lymphoma Eur J Dermatol 13 2003 553 559
95. T. Kallinich, J.M. Muche, S. Qin, W. Sterry, H. Audring, and R.A. Kroczek Chemokine receptor expression on neoplastic and reactive T cells in the skin at different stages of mycosis fungoides J Invest Dermatol 121 2003 1045 1052
96. G. Saed, D.P. Fivenson, Y. Naidu, and B.J. Nickoloff Mycosis fungoides exhibits a Th1-type cell-mediated cytokine profile whereas Sézary syndrome expresses a Th2-type profile J Invest Dermatol 103 1994 29 33
97. V. Sigurdsson, J. Toonstra, I.C. Bihari, C.A. Bruijnzeel-Koomen, W.A. van Vloten, and T. Thepen Interleukin 4 and interferon-gamma expression of the dermal infiltrate in patients with erythroderma and mycosis fungoides. An immuno-histochemical study J Cutan Pathol 27 2000 429 435
98. B.F. Chong, A.J. Wilson, H.M. Gibson, M.S. Hafner, Y. Luo, and C.J. Hedgcock et al. Immune function abnormalities in peripheral blood mononuclear cell cytokine expression differentiates stages of cutaneous T-cell lymphoma/mycosis fungoides Clin Cancer Res 14 2008 646 653
99. R.A. Clark, R. Watanabe, J.E. Teague, C. Schlapbach, M.C. Tawa, and N. Adams et al. Skin effector memory T cells do not recirculate and provide immune protection in alemtuzumab-treated CTCL patients Sci Transl Med 4 2012 117ra7
100. J.J. Campbell, R.A. Clark, R. Watanabe, and T.S. Kupper Sézary syndrome and mycosis fungoides arise from distinct T-cell subsets: a biologic rationale for their distinct clinical behaviors Blood 116 2010 767 771
101. X. Mao, G. Orchard, D.M. Lillington, F.J. Child, E.C. Vonderheid, and P.C. Nowell et al. BCL2 and JUNB abnormalities in primary cutaneous lymphomas Br J Dermatol 151 2004 546 556
102. X. Mao, G. Orchard, D.M. Lillington, R. Russell-Jones, B.D. Young, and S.J. Whittaker Amplification and overexpression of JUNB is associated with primary cutaneous T-cell lymphomas Blood 101 2003 1513 1519
103. X. Mao, G. Orchard, T.J. Mitchell, N. Oyama, R. Russell-Jones, and M.H. Vermeer 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
104. M. Nielsen, C.G. Kaestel, K.W. Eriksen, A. Woetmann, T. Stokkedal, and K. Kaltoft et al. Inhibition of constitutively activated Stat3 correlates with altered Bcl-2/Bax expression and induction of apoptosis in mycosis fungoides tumor cells Leukemia 13 1999 735 738
105. V.H. Sommer, O.J. Clemmensen, O. Nielsen, M. Wasik, P. Lovato, and C. Brender et al. In vivo activation of STAT3 in cutaneous T-cell lymphoma. Evidence for an antiapoptotic function of STAT3 Leukemia 18 2004 1288 1295
106. I.C. Navas, P.L. Ortiz-Romero, R. Villuendas, P. Martinez, C. Garcia, and E. Gomez et al. p16(INK4a) gene alterations are frequent in lesions of mycosis fungoides Am J Pathol 156 2000 1565 1572
107. X. Mao, G. Orchard, E.C. Vonderheid, P.C. Nowell, M. Bagot, and A. Bensussan et al. Heterogeneous abnormalities of CCND1 and RB1 in primary cutaneous T-Cell lymphomas suggesting impaired cell cycle control in disease pathogenesis J Invest Dermatol 126 2006 1388 1395
108. J.J. Scarisbrick, A.J. Woolford, E. Calonje, A. Photiou, S. Ferreira, and G. Orchard et al. Frequent abnormalities of the p15 and p16 genes in mycosis fungoides and Sézary syndrome J Invest Dermatol 118 2002 493 499
109. E. Laharanne, E. Chevret, Y. Idrissi, C. Gentil, M. Longy, and J. Ferrer et al. CDKN2A-CDKN2B deletion defines an aggressive subset of cutaneous T-cell lymphoma Mod Pathol 23 2010 547 558
110. R. van Doorn, W.H. Zoutman, R. Dijkman, R.X. de Menezes, S. Commandeur, and A.A. Mulder et al. Epigenetic profiling of cutaneous T-cell lymphoma: promoter hypermethylation of multiple tumor suppressor genes including BCL7a, PTPRG, and p73 J Clin Oncol 23 2005 3886 3896
111. X. Mao, D. Lillington, J.J. Scarisbrick, T. Mitchell, B. Czepulkowski, and R. Russell-Jones et al. Molecular cytogenetic analysis of cutaneous T-cell lymphomas: identification of common genetic alterations in Sézary syndrome and mycosis fungoides Br J Dermatol 147 2002 464 475
112. J.J. Scarisbrick, A.J. Woolford, R. Russell-Jones, and S.J. Whittaker Loss of heterozygosity on 10q and microsatellite instability in advanced stages of primary cutaneous T-cell lymphoma and possible association with homozygous deletion of PTEN Blood 95 2000 2937 2942
113. E. Contassot, K. Kerl, S. Roques, R. Shane, O. Gaide, and M. Dupuis et al. Resistance to FasL and tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis in Sézary syndrome T-cells associated with impaired death receptor and FLICE-inhibitory protein expression Blood 111 2008 4780 4787
114. O. Dereure, E. Levi, E.C. Vonderheid, and M.E. Kadin Infrequent Fas mutations but no Bax or p53 mutations in early mycosis fungoides: a possible mechanism for the accumulation of malignant T lymphocytes in the skin J Invest Dermatol 118 2002 949 956
115. + T lymphocytes in cutaneous T-cell lymphomas Br J Dermatol 143 2000 1205 1210
116. J. Wu, M. Nihal, J. Siddiqui, E.C. Vonderheid, and G.S. Wood Low FAS/CD95 expression by CTCL correlates with reduced sensitivity to apoptosis that can be restored by FAS upregulation J Invest Dermatol 129 2009 1165 1173
117. C.L. Jones, E.M. Wain, C.C. Chu, I. Tosi, R. Foster, and R.C. McKenzie et al. Downregulation of Fas gene expression in Sézary syndrome is associated with promoter hypermethylation J Invest Dermatol 130 2010 1116 1125
118. R. van Doorn, R. Dijkman, M.H. Vermeer, T.M. Starink, R. Willemze, and C.P. Tensen A novel splice variant of the Fas gene in patients with cutaneous T-cell lymphoma Cancer Res 62 2002 5389 5392
119. U. Ralfkiaer, P.H. Hagedorn, N. Bangsgaard, M.B. Lovendorf, C.B. Ahler, and L. Svensson et al. Diagnostic microRNA profiling in cutaneous T-cell lymphoma (CTCL) Blood 118 2011 5891 5900
120. F. Cetinozman, P.M. Jansen, M.H. Vermeer, and R. Willemze Differential expression of Programmed Death-1 (PD-1) in Sézary syndrome and mycosis fungoides Arch Dermatol 148 2012 1379 1385
121. + T cells in cutaneous T-cell lymphoma: implications for immune suppression Arch Dermatol 146 2010 1382 1388
122. R. van Doorn, E. Scheffer, and R. Willemze Follicular mycosis fungoides, a distinct disease entity with or without associated follicular mucinosis: a clinicopathologic and follow-up study of 51 patients Arch Dermatol 138 2002 191 198
123. C. Muniesa, T. Estrach, R.M. Pujol, F. Gallardo, P. Garcia-Muret, and J. Climent et al. Folliculotropic mycosis fungoides: clinicopathological features and outcome in a series of 20 cases J Am Acad Dermatol 62 2010 418 426
124. B. Haghighi, B.R. Smoller, P.E. LeBoit, R.A. Warnke, C.A. Sander, and S. Kohler Pagetoid reticulosis (Woringer-Kolopp disease): an immunophenotypic, molecular, and clinicopathologic study Mod Pathol 13 2000 502 510
125. A. Scarabello, B. Leinweber, M. Ardigo, A. Rutten, A.C. Feller, and H. Kerl et al. Cutaneous lymphomas with prominent granulomatous reaction: a potential pitfall in the histopathologic diagnosis of cutaneous T- and B-cell lymphomas Am J Surg Pathol 26 2002 1259 1268
126. F. Gallardo, M.P. Garcia-Muret, O. Servitje, T. Estrach, I. Bielsa, and A. Salar et al. Cutaneous lymphomas showing prominent granulomatous component: clinicopathological features in a series of 16 cases J Eur Acad Dermatol Venereol 23 2009 639 647
127. J. Li, M.P. Pulitzer, P.L. Myskowski, S.W. Dusza, S. Horwitz, and A. Moskowitz et al. A case-control study of clinicopathologic features, prognosis, and therapeutic responses in patients with granulomatous mycosis fungoides J Am Acad Dermatol 69 2013 366 374
128. W. Kempf, S. Ostheeren-Michaelis, M. Paulli, M. Lucioni, J. Wechsler, and H. Audring et al. Granulomatous mycosis fungoides and granulomatous slack skin: a multicenter study of the Cutaneous Lymphoma Histopathology Task Force Group of the European Organization For Research and Treatment of Cancer (EORTC) Arch Dermatol 144 2008 1609 1617
129. S.O. Arulogun, H.M. Prince, J. Ng, S. Lade, G.F. Ryan, and O. Blewitt et al. Long-term outcomes of patients with advanced-stage cutaneous T-cell lymphoma and large cell transformation Blood 112 2008 3082 3087
130. M.F. Benner, P.M. Jansen, M.H. Vermeer, and R. Willemze Prognostic factors in transformed mycosis fungoides: a retrospective analysis of 100 cases Blood 119 2012 1643 1649
131. E. Diamandidou, M. Colome-Grimmer, L. Fayad, M. Duvic, and R. Kurzrock Transformation of mycosis fungoides/Sézary syndrome: clinical characteristics and prognosis Blood 92 1998 1150 1159
132. B. Vergier, A. de Muret, M. Beylot-Barry, L. Vaillant, D. Ekouevi, and G. Chene et al. Transformation of mycosis fungoides: clinicopathological and prognostic features of 45 cases. French Study Group of Cutaneious Lymphomas Blood 95 2000 2212 2218
133. J.L. Herrmann, and L.C. Hughey Recognizing large-cell transformation of mycosis fungoides J Am Acad Dermatol 67 2012 665 672