Psoralen plus ultraviolet A ± interferon-α treatment resistance in mycosis fungoides: The role of tumour microenvironment, nuclear transcription factor-κB and T-cell receptor pathways

British Journal of Dermatology

Volumn 160, Issue 1, 2009, Pages 92-102

  Wozniak, M B ^a   Tracey, L ^a   Ortiz Romero, P L ^b   Montes, S ^b   Alvarez, M ^c   Fraga, J ^d   Fernandez Herrera J ^d   Vidal, S ^e   Rodriguez Peralto, J L ^b   Piris, M A ^a   Villuendas, R ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^c HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

^d HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

^e HOSPITAL CENTRAL DE LA DEFENSA GÓMEZ ULLA   (Spain)

Author keywords

Interferon alpha; Microarray analysis; Microenvironment; Mycosis fungoides; Psoralen plus ultraviolet A

Indexed keywords

ALPHA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PSORALEN; T LYMPHOCYTE RECEPTOR;

ADULT; AGED; ARTICLE; CANCER STAGING; CELL PROLIFERATION; CELL SUBPOPULATION; CELL SURVIVAL; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DENDRITIC CELL; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MICROENVIRONMENT; MYCOSIS FUNGOIDES; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; TREATMENT OUTCOME; TREATMENT RESPONSE; ULTRAVIOLET A RADIATION;

ADOLESCENT; ADULT; AGED; COMBINED MODALITY THERAPY; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; INTERFERON-ALPHA; MALE; MIDDLE AGED; MYCOSIS FUNGOIDES; NF-KAPPA B; PUVA THERAPY; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 57649197950     PISSN: 00070963     EISSN: 13652133     Source Type: Journal    
DOI: 10.1111/j.1365-2133.2008.08886.x     Document Type: Article

References (45)

1. Edelson RL. Cutaneous T cell lymphoma: mycosis fungoides, Sézary syndrome, and other variants. J Am Acad Dermatol 1980 2 : 89 106.
2. Girardi M, Heald PW, Wilson LD. The pathogenesis of mycosis fungoides. N Engl J Med 2004 350 : 1978 88.
3. Siegel RS, Pandolfino T, Guitart J et al. Primary cutaneous T-cell lymphoma: review and current concepts. J Clin Oncol 2000 18 : 2908 25.
4. Caffieri S, Di Lisa F, Bolesani F et al. The mitochondrial effects of novel apoptogenic molecules generated by psoralen photolysis as a crucial mechanism in PUVA therapy. Blood 2007 109 : 4988 94.
5. Stark GR, Kerr IM, Williams BR et al. How cells respond to interferons. Annu Rev Biochem 1998 67 : 227 64.
6. Xie RL, Gupta S, Miele A et al. The tumor suppressor interferon regulatory factor 1 interferes with SP1 activation to repress the human CDK2 promoter. J Biol Chem 2003 278 : 26589 96.
7. Olsen EA. Interferon in the treatment of cutaneous T-cell lymphoma. Dermatol Ther 2003 16 : 311 21.
8. Chiarion-Sileni V, Bononi A, Fornasa CV et al. Phase II trial of interferon-alpha-2a plus psolaren with ultraviolet light A in patients with cutaneous T-cell lymphoma. Cancer 2002 95 : 569 75.
9. Rupoli S, Goteri G, Pulini S et al. Long-term experience with low-dose interferon-alpha and PUVA in the management of early mycosis fungoides. Eur J Haematol 2005 75 : 136 45.
10. Stadler RKA, Luger T, Sterry W. Prospective, randomized, multicentre clinical trial on the use of interferon a-2a plus PUVA versus PUVA monotherapy in patients with cutaneous T-cell lymphoma, stages I and II. J Clin Oncology, ASCO Annual Meeting Proceedings Part I 2006 24 (Suppl. 18s. (abstr 7541).
11. Colamonici OR, Domanski P, Platanias LC et al. Correlation between interferon (IFN) alpha resistance and deletion of the IFN alpha/beta genes in acute leukemia cell lines suggests selection against the IFN system. Blood 1992 80 : 744 9.
12. Landolfo S, Guarini A, Riera L et al. Chronic myeloid leukemia cells resistant to interferon-alpha lack STAT1 expression. Hematol J 2000 1 : 7 14.
13. Gamero AM, Sakamoto S, Montenegro J et al. Identification of a novel conserved motif in the STAT family that is required for tyrosine phosphorylation. J Biol Chem 2004 279 : 12379 85.
14. Roman-Gomez J, Jimenez-Velasco A, Castillejo JA et al. The suppressor of cytokine signaling-1 is constitutively expressed in chronic myeloid leukemia and correlates with poor cytogenetic response to interferon-alpha. Haematologica 2004 89 : 42 8.
15. Yang CH, Murti A, Pfeffer LM. STAT3 complements defects in an interferon-resistant cell line: evidence for an essential role for STAT3 in interferon signaling and biological activities. Proc Natl Acad Sci U S A 1998 95 : 5568 72.
16. Sun WH, Pabon C, Alsayed Y et al. Interferon-alpha resistance in a cutaneous T-cell lymphoma cell line is associated with lack of STAT1 expression. Blood 1998 91 : 570 6.
17. Abramovich C, Shulman LM, Ratovitski E et al. Differential tyrosine phosphorylation of the IFNAR chain of the type I interferon receptor and of an associated surface protein in response to IFN-alpha and IFN-beta. EMBO J 1994 13 : 5871 7.
18. McKendry R, John J, Flavell D et al. High-frequency mutagenesis of human cells and characterization of a mutant unresponsive to both alpha and gamma interferons. Proc Natl Acad Sci U S A 1991 88 : 11455 9.
19. Sakamoto H, Yasukawa H, Masuhara M et al. A Janus kinase inhibitor, JAB, is an interferon-gamma-inducible gene and confers resistance to interferons. Blood 1998 92 : 1668 76.
20. Tracey L, Villuendas R, Ortiz P et al. Identification of genes involved in resistance to interferon-alpha in cutaneous T-cell lymphoma. Am J Pathol 2002 161 : 1825 37.
21. Tracey L, Spiteri I, Ortiz P et al. Transcriptional response of T cells to IFN-alpha: changes induced in IFN-alpha-sensitive and resistant cutaneous T cell lymphoma. J Interferon Cytokine Res 2004 24 : 185 95.
22. Nanbo A, Inoue K, Adachi-Takasawa K et al. Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt's lymphoma. EMBO J 2002 21 : 954 65.
23. Tracey L, Villuendas R, Dotor AM et al. Mycosis fungoides shows concurrent deregulation of multiple genes involved in the TNF signaling pathway: an expression profile study. Blood 2003 102 : 1042 50.
24. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001 98 : 5116 21.
25. Mootha VK, Lindgren CM, Eriksson KF et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003 34 : 267 73.
26. Subramanian A, Tamayo P, Mootha VK et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005 102 : 15545 50.
27. Rodríguez A, Martínez N, Camacho FI et al. Variability in the degree of expression of phosphorylated IkappaBalpha in chronic lymphocytic leukemia cases with nodal involvement. Clin Cancer Res 2004 10 : 6796 806.
28. Zhou Y, Wang S, Gobl A et al. The interferon-alpha regulation of interferon regulatory factor 1 (IRF-1) and IRF-2 has therapeutic implications in carcinoid tumors. Ann Oncol 2000 11 : 707 14.
29. Wolf P, Nghiem DX, Walterscheid JP et al. Platelet-activating factor is crucial in psoralen and ultraviolet A-induced immune suppression, inflammation, and apoptosis. Am J Pathol 2006 169 : 795 805.
30. Kim-Han JS, Reichert SA, Quick KL et al. BMCP1: a mitochondrial uncoupling protein in neurons which regulates mitochondrial function and oxidant production. J Neurochem 2001 79 : 658 68.
31. Raccurt M, Tam SP, Lau P et al. Suppressor of cytokine signalling gene expression is elevated in breast carcinoma. Br J Cancer 2003 89 : 524 32.
32. Herreros B, Sanchez-Aguilera A, Piris MA. Lymphoma microenvironment: culprit or innocent? Leukemia 2008 22 : 49 58.
33. Galmarini CM, Galmarini FC. Multidrug resistance in cancer therapy: role of the microenvironment. Curr Opin Investig Drugs 2003 4 : 1416 21.
34. Li ZW, Dalton WS. Tumor microenvironment and drug resistance in hematologic malignancies. Blood Rev 2006 20 : 333 42.
35. Shurin MR, Shurin GV, Lokshin A et al. Intratumoral cytokines/chemokines/ growth factors and tumor infiltrating dendritic cells: friends or enemies? Cancer Metastasis Rev 2006 25 : 333 56.
36. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005 7 : 211 17.
37. Zhang Q, Nowak I, Vonderheid EC et al. Activation of Jak/STAT proteins involved in signal transduction pathway mediated by receptor for interleukin 2 in malignant T lymphocytes derived from cutaneous anaplastic large T-cell lymphoma and Sézary syndrome. Proc Natl Acad Sci U S A 1996 93 : 9148 53.
38. Göthert JR, Brake RL, Smeets M et al. NOTCH1 pathway activation is an early hallmark of SCL T leukemogenesis. Blood 2007 110 : 3753 62.
39. Nefedova Y, Cheng P, Alsina M et al. Involvement of Notch-1 signaling in bone marrow stroma-mediated de novo drug resistance of myeloma and other malignant lymphoid cell lines. Blood 2004 103 : 3503 10.
40. Sommer VH, Clemmensen OJ, Nielsen O et al. In vivo activation of STAT3 in cutaneous T-cell lymphoma. Evidence for an antiapoptotic function of STAT3. Leukemia 2004 18 : 1288 95.
41. Takeda K, Clausen BE, Kaisho T et al. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 1999 10 : 39 49.
42. Brender C, Nielsen M, Kaltoft K et al. STAT3-mediated constitutive expression of SOCS-3 in cutaneous T-cell lymphoma. Blood 2001 97 : 1056 62.
43. Whittaker S. Biological insights into the pathogenesis of cutaneous T-cell lymphomas (CTCL). Semin Oncol 2006 33 : S3 6.
44. Bhardwaj A, Sethi G, Vadhan-Raj S et al. Resveratrol inhibits proliferation, induces apoptosis, and overcomes chemoresistance through down-regulation of STAT3 and nuclear factor-kappaB-regulated antiapoptotic and cell survival gene products in human multiple myeloma cells. Blood 2007 109 : 2293 302.
45. Sors A, Jean-Louis F, Pellet C et al. Down-regulating constitutive activation of the NF-kappaB canonical pathway overcomes the resistance of cutaneous T-cell lymphoma to apoptosis. Blood 2006 107 : 2354 63.