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Review | Open Access

Epigenetics of cutaneous T-cell lymphoma: biomarkers and therapeutic potentials

Pan Lai, Yang Wang ( )
Department of Dermatology and Venereology, Peking University First Hospital, Beijing Key Laboratory of Molecular Diagnosis on Dermatoses, National Clinical Research Center for Skin and Immune Diseases, Beijing 100034, China
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Abstract

Cutaneous T-cell lymphomas (CTCLs) are a heterogeneous group of skin-homing non-Hodgkin lymphomas. There are limited options for effective treatment of patients with advanced-stage CTCL, leading to a poor survival rate. Epigenetics plays a pivotal role in regulating gene expression without altering the DNA sequence. Epigenetic alterations are involved in virtually all key cancer-associated pathways and are fundamental to the genesis of cancer. In recent years, the epigenetic hallmarks of CTCL have been gradually elucidated and their potential values in the diagnosis, prognosis, and therapeutic intervention have been clarified. In this review, we summarize the current knowledge of the best-studied epigenetic modifications in CTCL, including DNA methylation, histone modifications, microRNAs, and chromatin remodelers. These epigenetic regulators are essential in the development of CTCL and provide new insights into the clinical treatments of this refractory disease.

Keywords

microRNADNA methylationEpigeneticshistone modificationcutaneous T-cell lymphomachromatin-remodeling complex

References

1

Willemze R, Cerroni L, Kempf W, Berti E, Facchetti F, Swerdlow SH, et al. The 2018 update of the WHO-EORTC classification for primary cutaneous lymphomas. Blood. 2019; 133: 1703-14.
Crossref Google Scholar
2

Agar NS, Wedgeworth E, Crichton S, Mitchell TJ, Cox M, Ferreira S, 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. 2010; 28: 4730-9.
Crossref Google Scholar
3

Kempf W, Pfaltz K, Vermeer MH, Cozzio A, Ortiz-Romero PL, Bagot M, et al. EORTC, ISCL, and USCLC consensus recommendations for the treatment of primary cutaneous CD30-positive lymphoproliferative disorders: lymphomatoid papulosis and primary cutaneous anaplastic large-cell lymphoma. Blood. 2011; 118: 4024-35.
Crossref Google Scholar
4

Gilson D, Whittaker SJ, Child FJ, Scarisbrick JJ, Illidge TM, Parry EJ, et al. British association of dermatologists and U.K. Cutaneous lymphoma group guidelines for the management of primary cutaneous lymphomas 2018. Br J Dermatol. 2019; 180: 496-526.
Crossref Google Scholar
5

Willemze R, Hodak E, Zinzani PL, Specht L, Ladetto M. Primary cutaneous lymphomas: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018; 29: iv30-40.
Crossref Google Scholar
6

Scarisbrick JJ, Prince HM, Vermeer MH, Quaglino P, Horwitz S, Porcu P, et al. Cutaneous Lymphoma International Consortium study of outcome in advanced stages of mycosis fungoides and Sézary syndrome: effect of specific prognostic markers on survival and development of a prognostic model. J Clin Oncol. 2015; 33: 3766-73.
Crossref Google Scholar
7

Quaglino P, Maule M, Prince HM, Porcu P, Horwitz S, Duvic M, et al. Global patterns of care in advanced stage mycosis fungoides/Sézary syndrome: a multicenter retrospective follow-up study from the Cutaneous Lymphoma International Consortium. Ann Oncol. 2019; 30: 494.
Crossref Google Scholar
8

Ungewickell A, Bhaduri A, Rios E, Reuter J, Lee CS, Mah A, et al. Genomic analysis of mycosis fungoides and Sézary syndrome identifies recurrent alterations in TNFR2. Nat Genet. 2015; 47: 1056-60.
Crossref Google Scholar
9

Park J, Yang J, Wenzel AT, Ramachandran A, Lee WJ, Daniels JC, et al. Genomic analysis of 220 CTCLs identifies a novel recurrent gain-of-function alteration in RLTPR (p.Q575E). Blood. 2017; 130: 1430-40.
Crossref Google Scholar
10

Vaque JP, Gomez-Lopez G, Monsalvez V, Varela I, Martinez N, Perez C, et al. PLCG1 mutations in cutaneous T-cell lymphomas. Blood. 2014; 123: 2034-43.
Crossref Google Scholar
11

Allis CD, Jenuwein T. The molecular hallmarks of epigenetic control. Nat Rev Genet. 2016; 17: 487-500.
Crossref Google Scholar
12

Taby R, Issa JP. Cancer epigenetics. CA Cancer J Clin. 2010; 60: 376-92.
Crossref Google Scholar
13

Kelly AD, Issa JJ. The promise of epigenetic therapy: reprogramming the cancer epigenome. Curr Opin Genet Dev. 2017; 42: 68-77.
Crossref Google Scholar
14

van Doorn R, Zoutman WH, Dijkman R, de Menezes RX, Commandeur S, Mulder AA, et al. Epigenetic profiling of cutaneous T-cell lymphoma: promoter hypermethylation of multiple tumor suppressor genes including BCL7a, PTPRG, and p73. J Clin Oncol. 2005; 23: 3886-96.
Crossref Google Scholar
15

Kohnken R, Wen J, Mundy-Bosse B, McConnell K, Keiter A, Grinshpun L, et al. Diminished microRNA-29b level is associated with BRD4-mediated activation of oncogenes in cutaneous T-cell lymphoma. Blood. 2018; 131: 771-81.
Crossref Google Scholar
16

Li Y, Wang J, Yu M, Wang Y, Zhang H, Yin J, et al. SNF5 deficiency induces apoptosis resistance by repressing SATB1 expression in Sézary syndrome. Leuk Lymphoma. 2018; 59: 2405-13.
Crossref Google Scholar
17

Jones CL, Wain EM, Chu CC, Tosi I, Foster R, McKenzie RC, et al. Downregulation of Fas gene expression in Sézary syndrome is associated with promoter hypermethylation. J Invest Dermatol. 2010; 130: 1116-25.
Crossref Google Scholar
18

Kaminskas E, Farrell A, Abraham S, Baird A, Hsieh L-S, Lee S-L, et al. Approval summary: azacitidine for treatment of myelodysplastic syndrome subtypes. Clin Cancer Res. 2005; 11: 3604-8.
Crossref Google Scholar
19

Kantarjian HM, Thomas XG, Dmoszynska A, Wierzbowska A, Mazur G, Mayer J, et al. Multicenter, randomized, open-label, phase Ⅲ trial of decitabine versus patient choice, with physician advice, of either supportive care or low-dose cytarabine for the treatment of older patients with newly diagnosed acute myeloid leukemia. J Clin Oncol. 2012; 30: 2670-7.
Crossref Google Scholar
20

Mann BS, Johnson JR, Cohen MH, Justice R, Pazdur R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist. 2007; 12: 1247-52.
Crossref Google Scholar
21

Piekarz RL, Frye R, Turner M, Wright JJ, Allen SL, Kirschbaum MH, et al. Phase Ⅱ multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J Clin Oncol. 2009; 27: 5410-7.
Crossref Google Scholar
22

Greger V, Passarge E, Höpping W, Messmer E, Horsthemke B. Epigenetic changes may contribute to the formation and spontaneous regression of retinoblastoma. Hum Genet. 1989; 83: 155-8.
Crossref Google Scholar
23

Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature. 1983; 301: 89-92.
Crossref Google Scholar
24

Herman JG. Hypermethylation of tumor suppressor genes in cancer. Semin Cancer Biol. 1999; 9: 359-67.
Crossref Google Scholar
25

Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002; 16: 6-21.
Crossref Google Scholar
26

Jones PA, Laird PW. Cancer-epigenetics comes of age. Nat Genet. 1999; 21: 163-67.
Crossref Google Scholar
27

Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet. 2002; 3: 415-28.
Crossref Google Scholar
28

Lyko F. The DNA methyltransferase family: a versatile toolkit for epigenetic regulation. Nat Rev Genet. 2018; 19: 81-92.
Crossref Google Scholar
29

Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999; 99: 247-57.
Crossref Google Scholar
30

Sen GL, Reuter JA, Webster DE, Zhu L, Khavari PA. DNMT1 maintains progenitor function in self-renewing somatic tissue. Nature. 2010; 463: 563-7.
Crossref Google Scholar
31

Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M, et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet. 2007; 39: 457-66.
Crossref Google Scholar
32

Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, et al. Initial sequencing and analysis of the human genome. Nature. 2001; 409: 860-921.
Crossref Google Scholar
33

Larsen F, Gundersen G, Lopez R, Prydz H. Cpg islands as gene markers in the human genome. Genomics. 1992; 13: 1095-107.
Crossref Google Scholar
34

Bird A, Taggart M, Frommer M, Miller OJ, Macleod D. A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA. Cell. 1985; 40: 91-9.
Crossref Google Scholar
35

Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med. 2003; 349: 2042-54.
Crossref Google Scholar
36

Navas IC, Ortiz-Romero PL, Villuendas R, Martinez P, Garcia C, Gomez E, et al. p16(INK4A) gene alterations are frequent in lesions of mycosis fungoides. Am J Pathol. 2000; 156: 1565-72.
Crossref Google Scholar
37

Ferrara G, Pancione M, Votino C, Quaglino P, Tomasini C, Santucci M, et al. A specific DNA methylation profile correlates with a high risk of disease progression in stage I classical (Alibert-Bazin type) mycosis fungoides. Br J Dermatol. 2014; 170: 1266-75.
Crossref Google Scholar
38

Wu J, Wood GS. Reduction of Fas/CD95 promoter methylation, upregulation of Fas protein, and enhancement of sensitivity to apoptosis in cutaneous T-cell lymphoma. Arch Dermatol. 2011; 147: 443-9.
Crossref Google Scholar
39

Novelli M, Fava P, Sarda C, Ponti R, Osella-Abate S, Savoia P, et al. Blood flow cytometry in Sézary syndrome: new insights on prognostic relevance and immunophenotypic changes during follow-up. Am J Clin Pathol. 2015; 143: 57-69.
Crossref Google Scholar
40

Scarisbrick JJ, Mitchell TJ, Calonje E, Orchard G, Russell-Jones R, Whittaker SJ. Microsatellite instability is associated with hypermethylation of the hMLH1 gene and reduced gene expression in mycosis fungoides. J Invest Dermatol. 2003; 121: 894-901.
Crossref Google Scholar
41

Witkiewicz A, Raghunath P, Wasik A, Junkins-Hopkins JM, Jones D, Zhang Q, et al. Loss of SHP-1 tyrosine phosphatase expression correlates with the advanced stages of cutaneous T-cell lymphoma. Hum Pathol. 2007; 38: 462-7.
Crossref Google Scholar
42

Zhang Q, Raghunath PN, Vonderheid E, Odum N, Wasik MA. Lack of phosphotyrosine phosphatase SHP-1 expression in malignant T-cell lymphoma cells results from methylation of the SHP-1 promoter. Am J Pathol. 2000; 157: 1137-46.
Crossref Google Scholar
43

Sommer VH, Clemmensen OJ, Nielsen O, Wasik M, Lovato P, Brender C, et al. In vivo activation of STAT3 in cutaneous T-cell lymphoma. Evidence for an antiapoptotic function of STAT3. Leukemia. 2004; 18: 1288-95.
Crossref Google Scholar
44

Zhang Q, Wang HY, Marzec M, Raghunath PN, Nagasawa T, Wasik MA. STAT3- and DNA methyltransferase 1-mediated epigenetic silencing of SHP-1 tyrosine phosphatase tumor suppressor gene in malignant T lymphocytes. Proc Natl Acad Sci U S A. 2005; 102: 6948-53.
Crossref Google Scholar
45

Ni X, Zhang C, Talpur R, Duvic M. Resistance to activationinduced cell death and bystander cytotoxicity via the Fas/Fas ligand pathway are implicated in the pathogenesis of cutaneous T cell lymphomas. J Invest Dermatol. 2005; 124: 741-50.
Crossref Google Scholar
46

Lissy NA, Davis PK, Irwin M, Kaelin WG, Dowdy SF. A common E2f-1 and p73 pathway mediates cell death induced by TCR activation. Nature. 2000; 407: 642-5.
Crossref Google Scholar
47

van Doorn R, Slieker RC, Boonk SE, Zoutman WH, Goeman JJ, Bagot M, et al. Epigenomic analysis of Sézary syndrome defines patterns of aberrant DNA methylation and identifies diagnostic markers. J Invest Dermatol. 2016; 136: 1876-84.
Crossref Google Scholar
48

Su MW, Dorocicz I, Dragowska WH, Ho V, Li G, Voss N, et al. Aberrant expression of T-plastin in Sézary cells. Cancer Res. 2003; 63: 7122-7.
Google Scholar
49

Jones CL, Ferreira S, McKenzie RC, Tosi I, Caesar JA, Bagot M, et al. Regulation of T-plastin expression by promoter hypomethylation in primary cutaneous T-cell lymphoma. J Invest Dermatol. 2012; 132: 2042-9.
Crossref Google Scholar
50

Wong HK, Gibson H, Hake T, Geyer S, Frederickson J, Marcucci G, et al. Promoter-specific hypomethylation is associated with overexpression of PLS3, GATA6, and TWIST1 in the Sézary syndrome. J Invest Dermatol. 2015; 135: 2084-92.
Crossref Google Scholar
51

Kamijo H, Miyagaki T, Shishido-Takahashi N, Nakajima R, Oka T, Suga H, et al. Aberrant CD137 ligand expression induced by GATA6 overexpression promotes tumor progression in cutaneous T-cell lymphoma. Blood. 2018; 132: 1922-35.
Crossref Google Scholar
52

Wang Y, Gu X, Zhang G, Wang L, Wang T, Zhao Y, et al. SATB1 overexpression promotes malignant T-cell proliferation in cutaneous CD30+ lymphoproliferative disease by repressing p21. Blood. 2014; 123: 3452-61.
Crossref Google Scholar
53

Jia Q, Wu W, Wang Y, Alexander PB, Sun C, Gong Z, et al. Local mutational diversity drives intratumoral immune heterogeneity in non-small cell lung cancer. Nat Commun. 2018; 9: 5361.
Crossref Google Scholar
54

Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009; 324: 930-5.
Crossref Google Scholar
55

Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science. 2009; 324: 929-30.
Crossref Google Scholar
56

Rasmussen KD, Helin K. Role of TET enzymes in DNA methylation, development, and cancer. Genes Dev. 2016; 30: 733-50.
Crossref Google Scholar
57

Qiu L, Liu F, Yi S, Li X, Liu X, Xiao C, et al. Loss of 5-hydroxymethylcytosine is an epigenetic biomarker in cutaneous T-cell lymphoma. J Invest Dermatol. 2018; 138: 2388-97.
Crossref Google Scholar
58

De Souza A, Tinguely M, Pfaltz M, Burghart DR, Kempf W. Loss of expression of 5-hydroxymethylcytosine in CD30-positive cutaneous lymphoproliferative disorders. J Cutan Pathol. 2014; 41: 901-6.
Crossref Google Scholar
59

da Silva Almeida AC, Abate F, Khiabanian H, Martinez-Escala E, Guitart J, Tensen CP, et al. The mutational landscape of cutaneous T cell lymphoma and Sézary syndrome. Nat Genet. 2015; 47: 1465-70.
Crossref Google Scholar
60

Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell. 2004; 116: 259-72.
Crossref Google Scholar
61

Richmond TJ, Davey CA. The structure of DNA in the nucleosome core. Nature. 2003; 423: 145-50.
Crossref Google Scholar
62

Jenuwein T, Allis CD. Translating the histone code. Science. 2001; 293: 1074-80.
Crossref Google Scholar
63

Pradeepa MM, Grimes GR, Kumar Y, Olley G, Taylor GC, Schneider R, et al. Histone H3 globular domain acetylation identifies a new class of enhancers. Nat Genet. 2016; 48: 681-6.
Crossref Google Scholar
64

Kouzarides T. Chromatin modifications and their function. Cell. 2007; 128: 693-705.
Crossref Google Scholar
65

Kebede AF, Schneider R, Daujat S. Novel types and sites of histone modifications emerge as players in the transcriptional regulation contest. FEBS J. 2015; 282: 1658-74.
Crossref Google Scholar
66

Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000; 403: 41-5.
Crossref Google Scholar
67

Tessarz P, Kouzarides T. Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol. 2014; 15: 703-8.
Crossref Google Scholar
68

Brunmeir R, Xu F. Functional regulation of PPARs through posttranslational modifications. Int J Mol Sci. 2018; 19: 1738.
Crossref Google Scholar
69

Park PJ. ChIP-seq: advantages and challenges of a maturing technology. Nat Rev Genet. 2009; 10: 669-80.
Crossref Google Scholar
70

Struhl K. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev. 1998; 12: 599-606.
Crossref Google Scholar
71

Ashburner BP, Westerheide SD, Baldwin AS, Jr. The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol Cell Biol. 2001; 21: 7065-77.
Crossref Google Scholar
72

Ikenoue T, Inoki K, Zhao B, Guan KL. PTEN acetylation modulates its interaction with PDZ domain. Cancer Res. 2008; 68: 6908-12.
Crossref Google Scholar
73

Lee DY, Hayes JJ, Pruss D, Wolffe AP. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell. 1993; 72: 73-84.
Crossref Google Scholar
74

Barneda-Zahonero B, Parra M. Histone deacetylases and cancer. Mol Oncol. 2012; 6: 579-89.
Crossref Google Scholar
75

Yi S, Sun J, Qiu L, Fu W, Wang A, Liu X, et al. Dual role of EZH2 in cutaneous anaplastic large cell lymphoma: promoting tumor cell survival and regulating tumor microenvironment. J Invest Dermatol. 2018; 138: 1126-36.
Crossref Google Scholar
76

Byvoet P, Shepherd GR, Hardin JM, Noland BJ. The distribution and turnover of labeled methyl groups in histone fractions of cultured mammalian cells. Arch Biochem Biophys. 1972; 148: 558-67.
Crossref Google Scholar
77

Greer EL, Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet. 2012; 13: 343-57.
Crossref Google Scholar
78

Esteller M. Epigenetics in cancer. N Engl J Med. 2008; 358: 1148-59.
Crossref Google Scholar
79

Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 2004; 119: 941-53.
Crossref Google Scholar
80

Wobser M, Weber A, Glunz A, Tauch S, Seitz K, Butelmann T, et al. Elucidating the mechanism of action of domatinostat (4SC-202) in cutaneous T cell lymphoma cells. J Hematol Oncol. 2019; 12: 30.
Crossref Google Scholar
81

Comet I, Riising EM, Leblanc B, Helin K. Maintaining cell identity: PRC2-mediated regulation of transcription and cancer. Nat Rev Cancer. 2016; 16: 803-10.
Crossref Google Scholar
82

Ernst T, Chase AJ, Score J, Hidalgo-Curtis CE, Bryant C, Jones AV, et al. Inactivating mutations of the histone methyltransferase gene EZH2 in myeloid disorders. Nat Genet. 2010; 42: 722-6.
Crossref Google Scholar
83

Aries IM, Bodaar K, Karim SA, Chonghaile TN, Hinze L, Burns MA, et al. PRC2 loss induces chemoresistance by repressing apoptosis in T cell acute lymphoblastic leukemia. J Exp Med. 2018; 215: 3094-114.
Crossref Google Scholar
84

McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature. 2012; 492: 108-12.
Crossref Google Scholar
85

Italiano A, Soria JC, Toulmonde M, Michot JM, Lucchesi C, Varga A, et al. Tazemetostat, an EZH2 inhibitor, in relapsed or refractory B-cell non-Hodgkin lymphoma and advanced solid tumours: a first-in-human, open-label, phase 1 study. Lancet Oncol. 2018; 19: 649-59.
Crossref Google Scholar
86

Yap TA, Winter JN, Giulino-Roth L, Longley J, Lopez J, Michot JM, et al. Phase I study of the novel enhancer of zeste homolog 2 (EZH2) inhibitor GSK2816126 in patients with advanced hematologic and solid tumors. Clin Cancer Res. 2019; 25: 7331-9.
Crossref Google Scholar
87

Brach D, Johnston-Blackwell D, Drew A, Lingaraj T, Motwani V, Warholic NM, et al. EZH2 inhibition by Tazemetostat results in altered dependency on B-cell activation signaling in DLBCL. Mol Cancer Ther. 2017; 16: 2586-97.
Crossref Google Scholar
88

Yamagishi M, Hori M, Fujikawa D, Ohsugi T, Honma D, Adachi N, et al. Targeting excessive EZH1 and EZH2 activities for abnormal histone methylation and transcription network in malignant lymphomas. Cell Rep. 2019; 29: 2321-37.e7.
Crossref Google Scholar
89

Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116: 281-97.
Crossref Google Scholar
90

Lai EC. microRNAs: runts of the genome assert themselves. Curr Biol. 2003; 13: R925-36.
Crossref Google Scholar
91

Chen CZ. MicroRNAs as oncogenes and tumor suppressors. N Engl J Med. 2005; 353: 1768-71.
Crossref Google Scholar
92

Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res. 2004; 14: 1902-10.
Crossref Google Scholar
93

Hammond SM, Bernstein E, Beach D, Hannon GJ. An RNAdirected nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature. 2000; 404: 293-6.
Crossref Google Scholar
94

Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med. 2009; 60: 167-79.
Crossref Google Scholar
95

Kohnken R, Mishra A. MicroRNAs in cutaneous T-cell lymphoma: the future of therapy. J Invest Dermatol. 2019; 139: 528-34.
Crossref Google Scholar
96

Metzler M, Wilda M, Busch K, Viehmann S, Borkhardt A. High expression of precursor microRNA-155/BIC RNA in children with Burkitt lymphoma. Genes Chromosomes Cancer. 2004; 39: 167-9.
Crossref Google Scholar
97

Sandoval J, Diaz-Lagares A, Salgado R, Servitje O, Climent F, Ortiz-Romero PL, et al. MicroRNA expression profiling and DNA methylation signature for deregulated microRNA in cutaneous T-cell lymphoma. J Invest Dermatol. 2015; 135: 1128-37.
Crossref Google Scholar
98

Moyal L, Barzilai A, Gorovitz B, Hirshberg A, Amariglio N, JacobHirsch J, et al. Mir-155 is involved in tumor progression of mycosis fungoides. Exp Dermatol. 2013; 22: 431-3.
Crossref Google Scholar
99

Seto AG, Beatty X, Lynch JM, Hermreck M, Tetzlaff M, Duvic M, et al. Cobomarsen, an oligonucleotide inhibitor of miR-155, co-ordinately regulates multiple survival pathways to reduce cellular proliferation and survival in cutaneous T-cell lymphoma. Br J Haematol. 2018; 183: 428-44.
Crossref Google Scholar
100

Fava P, Bergallo M, Astrua C, Brizio M, Galliano I, Montanari P, et al. miR-155 expression in primary cutaneous T-cell lymphomas (CTCL). J Eur Acad Dermatol Venereol. 2017; 31: e27-9.
Crossref Google Scholar
101

Fredholm S, Willerslev-Olsen A, Met O, Kubat L, Gluud M, Mathiasen SL, et al. SATB1 in malignant T cells. J Invest Dermatol. 2018; 138: 1805-15.
Crossref Google Scholar
102

Kopp KL, Ralfkiaer U, Gjerdrum LM, Helvad R, Pedersen IH, Litman T, et al. STAT5-mediated expression of oncogenic miR-155 in cutaneous T-cell lymphoma. Cell Cycle. 2013; 12: 1939-47.
Crossref Google Scholar
103

Moyal L, Yehezkel S, Gorovitz B, Keren A, Gilhar A, Lubin I, et al. Oncogenic role of microRNA-155 in mycosis fungoides: an in vitro and xenograft mouse model study. Br J Dermatol. 2017; 177: 791-800.
Crossref Google Scholar
104

Narducci MG, Arcelli D, Picchio MC, Lazzeri C, Pagani E, Sampogna F, et al. MicroRNA profiling reveals that miR-21, miR486 and miR-214 are upregulated and involved in cell survival in Sézary syndrome. Cell Death Dis. 2011; 2: e151.
Crossref Google Scholar
105

van der Fits L, van Kester MS, Qin Y, Out-Luiting JJ, Smit F, Zoutman WH, et al. MicroRNA-21 expression in CD4+ t cells is regulated by STAT3 and is pathologically involved in Sézary syndrome. J Invest Dermatol. 2011; 131: 762-8.
Crossref Google Scholar
106

Qin Y, Buermans HP, van Kester MS, van der Fits L, Out-Luiting JJ, Osanto S, et al. Deep-sequencing analysis reveals that the miR-199a2/214 cluster within DNM3os represents the vast majority of aberrantly expressed microRNAs in Sézary syndrome. J Invest Dermatol. 2012; 132: 1520-2.
Crossref Google Scholar
107

Kohnken R, McNeil B, Wen J, McConnell K, Grinshpun L, Keiter A, et al. Preclinical targeting of microRNA-214 in cutaneous T-cell lymphoma. J Invest Dermatol. 2019; 139: 1966-74.e3.
Crossref Google Scholar
108

An X, Sarmiento C, Tan T, Zhu H. Regulation of multidrug resistance by microRNAs in anti-cancer therapy. Acta Pharm Sin B. 2017; 7: 38-51.
Crossref Google Scholar
109

Manfe V, Biskup E, Rosbjerg A, Kamstrup M, Skov AG, Lerche CM, et al. miR-122 regulates p53/Akt signalling and the chemotherapyinduced apoptosis in cutaneous T-cell lymphoma. PLoS One. 2012; 7: e29541.
Crossref Google Scholar
110

Manfe V, Biskup E, Willumsgaard A, Skov AG, Palmieri D, Gasparini P, et al. cMyc/miR-125b-5p signalling determines sensitivity to bortezomib in preclinical model of cutaneous T-cell lymphomas. PLoS One. 2013; 8: e59390.
Crossref Google Scholar
111

Benner MF, Ballabio E, van Kester MS, Saunders NJ, Vermeer MH, Willemze R, et al. Primary cutaneous anaplastic large cell lymphoma shows a distinct miRNA expression profile and reveals differences from tumor-stage mycosis fungoides. Exp Dermatol. 2012; 21: 632-4.
Crossref Google Scholar
112

McGirt LY, Adams CM, Baerenwald DA, Zwerner JP, Zic JA, Eischen CM. miR-223 regulates cell growth and targets proto-oncogenes in mycosis fungoides/cutaneous T-cell lymphoma. J Invest Dermatol. 2014; 134: 1101-7.
Crossref Google Scholar
113

Zhang Y, Wang Y, Yu R, Huang Y, Su M, Xiao C, et al. Molecular markers of early-stage mycosis fungoides. J Invest Dermatol. 2012; 132: 1698-706.
Crossref Google Scholar
114

Ito M, Teshima K, Ikeda S, Kitadate A, Watanabe A, Nara M, et al. MicroRNA-150 inhibits tumor invasion and metastasis by targeting the chemokine receptor CCR6, in advanced cutaneous T-cell lymphoma. Blood. 2014; 123: 1499-511.
Crossref Google Scholar
115

Abe F, Kitadate A, Ikeda S, Yamashita J, Nakanishi H, Takahashi N, et al. Histone deacetylase inhibitors inhibit metastasis by restoring a tumor suppressive microRNA-150 in advanced cutaneous T-cell lymphoma. Oncotarget. 2017; 8: 7572-85.
Crossref Google Scholar
116

Gallardo F, Sandoval J, Diaz-Lagares A, Garcia R, D’Altri T, Gonzalez J, et al. Notch1 pathway activation results from the epigenetic abrogation of notch-related microRNAs in mycosis fungoides. J Invest Dermatol. 2015; 135: 3144-52.
Crossref Google Scholar
117

Kitadate A, Ikeda S, Teshima K, Ito M, Toyota I, Hasunuma N, et al. MicroRNA-16 mediates the regulation of a senescence-apoptosis switch in cutaneous T-cell and other non-Hodgkin lymphomas. Oncogene. 2016; 35: 3692-704.
Crossref Google Scholar
118

Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008; 18: 997-1006.
Crossref Google Scholar
119

Mohr AM, Mott JL. Overview of microRNA biology. Semin Liver Dis. 2015; 35: 3-11.
Crossref Google Scholar
120

Ralfkiaer U, Hagedorn PH, Bangsgaard N, Lovendorf MB, Ahler CB, Svensson L, et al. Diagnostic microRNA profiling in cutaneous T-cell lymphoma (CTCL). Blood. 2011; 118: 5891-900.
Crossref Google Scholar
121

Shen X, Wang B, Li K, Wang L, Zhao X, Xue F, et al. MicroRNA signatures in diagnosis and prognosis of cutaneous T-cell lymphoma. J Invest Dermatol. 2018; 138: 2024-32.
Crossref Google Scholar
122

Lindahl LM, Besenbacher S, Rittig AH, Celis P, Willerslev-Olsen A, Gjerdrum LMR, et al. Prognostic miRNA classifier in earlystage mycosis fungoides: development and validation in a Danish nationwide study. Blood. 2018; 131: 759-70.
Crossref Google Scholar
123

Marstrand T, Ahler CB, Ralfkiaer U, Clemmensen A, Kopp KL, Sibbesen NA, et al. Validation of a diagnostic microRNA classifier in cutaneous t-cell lymphomas. Leuk Lymphoma. 2014; 55: 957-8.
Crossref Google Scholar
124

Dusilkova N, Basova P, Polivka J, Kodet O, Kulvait V, Pesta M, et al. Plasma miR-155, miR-203, and miR-205 are biomarkers for monitoring of primary cutaneous T-cell lymphomas. Int J Mol Sci. 2017; 18: 2136.
Crossref Google Scholar
125

Kohler S, Kim YH, Smoller BR. Histologic criteria for the diagnosis of erythrodermic mycosis fungoides and Sézary syndrome: a critical reappraisal. J Cutan Pathol. 1997; 24: 292-7.
Crossref Google Scholar
126

Rittig AH, Lindahl LM, Johansen C, Celis P, Odum N, Iversen L, et al. The microRNA expression profile differs between erythrodermic mycosis fungoides and Sézary syndrome. Acta Derm Venereol. 2019; 99: 1148-53.
Crossref Google Scholar
127

Maj J, Jankowska-Konsur A, Sadakierska-Chudy A, Noga L, Reich A. Altered microRNA expression in mycosis fungoides. Br J Dermatol. 2012; 166: 331-6.
Crossref Google Scholar
128

Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem. 2009; 78: 273-304.
Crossref Google Scholar
129

Halliday GM, Bock VL, Moloney FJ, Lyons JG. SWI/SNF: a chromatin-remodelling complex with a role in carcinogenesis. Int J Biochem Cell Biol. 2009; 41: 725-8.
Crossref Google Scholar
130

Yasui D, Miyano M, Cai S, Varga-Weisz P, Kohwi-Shigematsu T. SATB1 targets chromatin remodelling to regulate genes over long distances. Nature. 2002; 419: 641-5.
Crossref Google Scholar
131

Wang Y, Su M, Zhou LL, Tu P, Zhang X, Jiang X, et al. Deficiency of SATB1 expression in Sézary cells causes apoptosis resistance by regulating FasL/CD95L transcription. Blood. 2011; 117: 3826-35.
Crossref Google Scholar
132

Grzanka A, Grzanka D, Gagat M, Tadrowski T, SokolowskaWojdylo M, Marszalek A, et al. Correlation of SATB1 expression with clinical course of cutaneous T-cell lymphomas. Pol J Pathol. 2012; 63: 101-5.
Google Scholar
133

Grzanka D, Gagat M, Izdebska M, Marszalek A. Expression of special AT-rich sequence-binding protein 1 is an independent prognostic factor in cutaneous T-cell lymphoma. Oncol Rep. 2015; 33: 250-66.
Crossref Google Scholar
134

Oki Y, Aoki E, Issa JP. Decitabine--bedside to bench. Crit Rev Oncol Hematol. 2007; 61: 140-52.
Crossref Google Scholar
135

Jain S, Washington A, Leaf RK, Bhargava P, Clark RA, Kupper TS, et al. Decitabine priming enhances mucin 1 inhibition mediated disruption of redox homeostasis in cutaneous T-cell lymphoma. Mol Cancer Ther. 2017; 16: 2304-14.
Crossref Google Scholar
136

Schcolnik-Cabrera A, Dominguez-Gomez G, Duenas-Gonzalez A. Comparison of DNA demethylating and histone deacetylase inhibitors hydralazine-valproate versus vorinostat-decitabine incutaneous T-cell lymphoma in HUT78 cells. Am J Blood Res. 2018; 8: 5-16.
Google Scholar
137

Wood GS, Wu J. Methotrexate and pralatrexate. Dermatol Clin. 2015; 33: 747-55.
Crossref Google Scholar
138

Grant S, Easley C, Kirkpatrick P. Vorinostat. Nat Rev Drug Discov. 2007; 6: 21-2.
Crossref Google Scholar
139

Foss F, Coiffier B, Horwitz S, Pro B, Prince HM, Sokol L, et al. Tolerability to romidepsin in patients with relapsed/refractory T-cell lymphoma. Biomark Res. 2014; 2: 16.
Crossref Google Scholar
140

Olsen EA, Kim YH, Kuzel TM, Pacheco TR, Foss FM, Parker S, et al. Phase Ⅱb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J Clin Oncol. 2007; 25: 3109-15.
Crossref Google Scholar
141

Bates SE, Eisch R, Ling A, Rosing D, Turner M, Pittaluga S, et al. Romidepsin in peripheral and cutaneous T-cell lymphoma: mechanistic implications from clinical and correlative data. Br J Haematol. 2015; 170: 96-109.
Crossref Google Scholar
142

Foss F, Advani R, Duvic M, Hymes KB, Intragumtornchai T, Lekhakula A, et al. A phase Ⅱ trial of belinostat (PXD101) in patients with relapsed or refractory peripheral or cutaneous T-cell lymphoma. Br J Haematol. 2015; 168: 811-9.
Crossref Google Scholar
143

Lee HZ, Kwitkowski VE, Del Valle PL, Ricci MS, Saber H, Habtemariam BA, et al. FDA approval: belinostat for the treatment of patients with relapsed or refractory peripheral T-cell lymphoma. Clin Cancer Res. 2015; 21: 2666-70.
Crossref Google Scholar
144

Shi Y, Dong M, Hong X, Zhang W, Feng J, Zhu J, et al. Results from a multicenter, open-label, pivotal phase Ⅱ study of chidamide in relapsed or refractory peripheral T-cell lymphoma. Ann Oncol. 2015; 26: 1766-71.
Crossref Google Scholar
145

Duvic M, Dummer R, Becker JC, Poulalhon N, Ortiz Romero P, Grazia Bernengo M, et al. Panobinostat activity in both bexaroteneexposed and -naive patients with refractory cutaneous T-cell lymphoma: results of a phase Ⅱ trial. Eur J Cancer. 2013; 49: 386-94.
Crossref Google Scholar
146

Tzogani K, van Hennik P, Walsh I, De Graeff P, Folin A, Sjöberg J, et al. EMA review of panobinostat (Farydak) for the treatment of adult patients with relapsed and/or refractory multiple myeloma. Oncologist. 2018; 23: 631-6.
Crossref Google Scholar
147

Duvic M, Kim YH, LeBoeuf NR, Porcu P, Hastings J, Bassuner J, et al. A phase 2 randomized study of SHAPE Gel (SHP-141) in patients with early-stage cutaneous T-cell lymphoma: interim results. J Clin Oncol. 2016; 34: 7562.
Crossref Google Scholar
148

Kim YH, Krathen M, Duvic M, Wong H, Porcu P, Tacastacas J, et al. A phase 1b study in cutaneous T-cell lymphoma (CTCL) with the novel topically applied skin-restricted histone deacteylase inhibitor (HDAC-i) SHP-141. J Clin Oncol. 2014; 32: 8525.
Crossref Google Scholar
149

Younes A, Berdeja JG, Patel MR, Flinn I, Gerecitano JF, Neelapu SS, et al. Safety, tolerability, and preliminary activity of CUDC-907, a first-in-class, oral, dual inhibitor of HDAC and PI3K, in patients with relapsed or refractory lymphoma or multiple myeloma: an open-label, dose-escalation, phase 1 trial. Lancet Oncol. 2016; 17: 622-31.
Crossref Google Scholar
150

Gardner JM, Introcaso CE, Nasta SD, Kim EJ, Vittorio CC, Rook AH. A novel regimen of vorinostat with interferon gamma for refractory Sézary syndrome. J Am Acad Dermatol. 2009; 61: 112-6.
Crossref Google Scholar
151

Samimi S, Morrissey K, Anshelevich S, Evans K, Gardner J, Musiek A, et al. Romidepsin and interferon gamma: a novel combination for refractory cutaneous T-cell lymphoma. J Am Acad Dermatol. 2013; 68: e5-6.
Crossref Google Scholar
152

Dummer R, Beyer M, Hymes K, Epping MT, Bernards R, Steinhoff M, et al. Vorinostat combined with bexarotene for treatment of cutaneous T-cell lymphoma: in vitro and phase I clinical evidence supporting augmentation of retinoic acid receptor/retinoid X receptor activation by histone deacetylase inhibition. Leuk Lymphoma. 2012; 53: 1501-8.
Crossref Google Scholar
153

Vu K, Wu CH, Yang CY, Zhan A, Cavallone E, Berry W, et al. Romidepsin plus liposomal doxorubicin is safe and effective in patients with relapsed or refractory T-cell lymphoma: results of a phase I dose-escalation study. Clin Cancer Res. 2020; 26: 1000-8.
Crossref Google Scholar
154

Querfeld C, Foss FM, Kim YH, Pinter-Brown L, William BM, Porcu P, et al. Phase 1 trial of cobomarsen, an inhibitor of MIR-155, in cutaneous T cell lymphoma. Blood. 2018; 132: 2903.
Crossref Google Scholar
155

Du J, Johnson LM, Jacobsen SE, Patel DJ. DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol. 2015; 16: 519-32.
Crossref Google Scholar
156

Bewersdorf JP, Shallis R, Stahl M, Zeidan AM. Epigenetic therapy combinations in acute myeloid leukemia: what are the options? Ther Adv Hematol. 2019; 10: 2040620718816698.
Crossref Google Scholar
157

Rozati S, Cheng PF, Widmer DS, Fujii K, Levesque MP, Dummer R. Romidepsin and azacitidine synergize in their epigenetic modulatory effects to induce apoptosis in CTCL. Clin Cancer Res. 2016; 22: 2020-31.
Crossref Google Scholar
158

Espinoza-Zamora JR, Labardini-Méndez J, Sosa-Espinoza A, López-González C, Vieyra-García M, Candelaria M, et al. Efficacy of hydralazine and valproate in cutaneous T-cell lymphoma, a phase Ⅱ study. Expert Opin Investig Drugs. 2017; 26: 481-7.
Crossref Google Scholar
159

Fu W, Yi S, Qiu L, Sun J, Tu P, Wang Y. BCL11B-mediated epigenetic repression is a crucial target for histone deacetylase inhibitors in cutaneous T-cell lymphoma. J Invest Dermatol. 2017; 137:1523-32.
Crossref Google Scholar
160

Andrews JM, Schmidt JA, Carson KR, Musiek AC, Mehta-Shah N, Payton JE. Novel cell adhesion/migration pathways are predictive markers of HDAC inhibitor resistance in cutaneous T cell lymphoma. EBioMedicine. 2019; 46: 170-83.
Crossref Google Scholar
161

Butler RM, McKenzie RC, Jones CL, Flanagan CE, Woollard WJ, Demontis M, et al. Contribution of STAT3 and RAD23B in primary Sézary cells to histone deacetylase inhibitor FK228 resistance. J Invest Dermatol. 2019; 139: 1975-84.e2.
Crossref Google Scholar
162

Qu K, Zaba LC, Satpathy AT, Giresi PG, Li R, Jin Y, et al. Chromatin accessibility landscape of cutaneous T cell lymphoma and dynamic response to HDAC inhibitors. Cancer Cell. 2017; 32: 27-41.e4.
Crossref Google Scholar
163

Buenrostro JD, Wu B, Chang HY, Greenleaf WJ. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr Protoc Mol Biol. 2015; 109: 21.29.1-21.29.9.
Crossref Google Scholar
164

Lu Y, Chan Y-T, Tan H-Y, Li S, Wang N, Feng Y. Epigenetic regulation in human cancer: the potential role of epi-drug in cancer therapy. Mol Cancer. 2020; 19: 79.
Crossref Google Scholar
165

Cao J, Yan Q. Cancer epigenetics, tumor immunity, and immunotherapy. Trends Cancer. 2020; 6: 580-92.
Crossref Google Scholar
166

Chiappinelli Katherine B, Strissel Pamela L, Desrichard A, Li H, Henke C, Akman B, et al. Inhibiting DNA methylation causes an interferon response in cancer via dsRNA including endogenous retroviruses. Cell. 2015; 162: 974-86.
Crossref Google Scholar
167

Peng D, Kryczek I, Nagarsheth N, Zhao L, Wei S, Wang W, et al. Epigenetic silencing of TH1-type chemokines shapes tumour immunity and immunotherapy. Nature. 2015; 527: 249-53.
Crossref Google Scholar
168

Liu L, Wang Y, Wu J, Liu J, Qin Z, Fan H. N(6)-Methyladenosine: a potential breakthrough for human cancer. Mol Ther Nucleic Acids. 2020; 19: 804-13.
Crossref Google Scholar
169

Shi H, Chai P, Jia R, Fan X. Novel insight into the regulatory roles of diverse RNA modifications: re-defining the bridge between transcription and translation. Mol Cancer. 2020; 19: 78.
Crossref Google Scholar
170

Amelio I, Bernassola F, Candi E. Emerging roles of long non-coding RNAs in breast cancer biology and management. Semin Cancer Biol. 2020; S1044-579X(20)30155-3.
Google Scholar
171

Lee CS, Ungewickell A, Bhaduri A, Qu K, Webster DE, Armstrong R, et al. Transcriptome sequencing in Sézary syndrome identifies Sézary cell and mycosis fungoides-associated lncRNAs and novel transcripts. Blood. 2012; 120: 3288-97.
Crossref Google Scholar
172

Gallardo F, Esteller M, Pujol RM, Costa C, Estrach T, Servitje O. Methylation status of the p15, p16 and MGMT promoter genes in primary cutaneous T-cell lymphomas. Haematologica. 2004; 89: 1401-3.
Google Scholar
173

de Silva S, Wang F, Hake TS, Porcu P, Wong HK, Wu L. Downregulation of SAMHD1 expression correlates with promoter DNA methylation in Sézary syndrome patients. J Invest Dermatol. 2014; 134: 562-5.
Crossref Google Scholar
174

Cristofoletti C, Picchio MC, Lazzeri C, Tocco V, Pagani E, Bresin A, et al. Comprehensive analysis of PTEN status in Sézary syndrome. Blood. 2013; 122: 3511-20.
Crossref Google Scholar
175

Ballabio E, Mitchell T, van Kester MS, Taylor S, Dunlop HM, Chi J, et al. MicroRNA expression in Sézary syndrome: identification, function, and diagnostic potential. Blood. 2010; 116: 1105-13.
Crossref Google Scholar
176

Kohnken R, Kodigepalli KM, Mishra A, Porcu P, Wu L. MicroRNA-181 contributes to downregulation of SAMHD1 expression in CD4+ T-cells derived from Sézary syndrome patients. Leuk Res. 2017; 52: 58-66.
Crossref Google Scholar
Cancer Biology & Medicine
Volume 18 Issue 1,
February 2021
Pages 34-51
DOI: 10.20892/j.issn.2095-3941.2020.0216
Cite this article:
Lai P, Wang Y. Epigenetics of cutaneous T-cell lymphoma: biomarkers and therapeutic potentials. Cancer Biology & Medicine, 2021, 18(1): 34-51. https://doi.org/10.20892/j.issn.2095-3941.2020.0216

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Received: 06 May 2020
Accepted: 30 July 2020
Published: 01 February 2021
©2021 Cancer Biology & Medicine.

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