Global long terminal repeat activation participates in establishing the unique gene expression programme of classical Hodgkin lymphoma.
Journal
Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895
Informations de publication
Date de publication:
06 2019
06 2019
Historique:
received:
09
03
2018
accepted:
29
10
2018
revised:
18
10
2018
pubmed:
14
12
2018
medline:
7
9
2019
entrez:
15
12
2018
Statut:
ppublish
Résumé
Long terminal repeat (LTR) elements are wide-spread in the human genome and have the potential to act as promoters and enhancers. Their expression is therefore under tight epigenetic control. We previously reported in classical Hodgkin Lymphoma (cHL) that a member of the THE1B class of LTR elements acted as a promoter for the proto-oncogene and growth factor receptor gene CSF1R and that expression of this gene is required for cHL tumour survival. However, to which extent and how such elements participate in globally shaping the unique cHL gene expression programme is unknown. To address this question we mapped the genome-wide activation of THE1-LTRs in cHL cells using a targeted next generation sequencing approach (RACE-Seq). Integration of these data with global gene expression data from cHL and control B cell lines showed a unique pattern of LTR activation impacting on gene expression, including genes associated with the cHL phenotype. We also show that global LTR activation is induced by strong inflammatory stimuli. Together these results demonstrate that LTR activation provides an additional layer of gene deregulation in classical Hodgkin lymphoma and highlight the potential impact of genome-wide LTR activation in other inflammatory diseases.
Identifiants
pubmed: 30546079
doi: 10.1038/s41375-018-0311-x
pii: 10.1038/s41375-018-0311-x
pmc: PMC6558280
mid: EMS80347
doi:
Substances chimiques
Biomarkers, Tumor
0
MAS1 protein, human
0
Proto-Oncogene Mas
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1463-1474Subventions
Organisme : Blood Cancer UK
ID : 15001
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M009157/1
Pays : United Kingdom
Références
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.
doi: 10.1038/35057062
Bannert N, Kurth R. The evolutionary dynamics of human endogenous retroviral families. Annu Rev Genom Hum Genet. 2006;7:149–73.
doi: 10.1146/annurev.genom.7.080505.115700
Glinsky GV. Transposable elements and DNA methylation create in embryonic stem cells human-specific regulatory sequences associated with distal enhancers and noncoding RNAs. Genome Biol Evol. 2015;7:1432–54.
doi: 10.1093/gbe/evv081
Babaian A, Mager DL. Endogenous retroviral promoter exaptation in human cancer. Mob DNA. 2016;7:24.
doi: 10.1186/s13100-016-0080-x
Lamprecht B, Walter K, Kreher S, Kumar R, Hummel M, Lenze D, et al. Derepression of an endogenous long terminal repeat activates the CSF1R proto-oncogene in human lymphoma. Nat Med. 2010;16:571–9. 1p following 9
doi: 10.1038/nm.2129
Kuppers R. The biology of Hodgkin’s lymphoma. Nat Rev Cancer. 2009;9:15–27.
doi: 10.1038/nrc2542
Loke J, Chin PS, Keane P, Pickin A, Assi SA, Ptasinska A, et al. C/EBPα overrides epigenetic reprogramming by oncogenic transcription factors in acute myeloid leukemia. Blood Adv. 2018;2:271–84.
doi: 10.1182/bloodadvances.2017012781
Obier N, Cauchy P, Assi SA, Gilmour J, Lie-A-Ling M, Lichtinger M, et al. Cooperative binding of AP-1 and TEAD4 modulates the balance between vascular smooth muscle and hemogenic cell fate. Development. 2016;143:4324-4340.
Lamprecht B, Walter K, Kreher S, Kumar R, Hummel M, Lenze D, et al. Derepression of an endogenous long terminal repeat activates the CSF1R proto-oncogene in human lymphoma. Nat Med. 2010;16:571–9.
doi: 10.1038/nm.2129
Fiumara P, Snell V, Li Y, Mukhopadhyay A, Younes M, Gillenwater AM, et al. Functional expression of receptor activator of nuclear factor kappaB in Hodgkin disease cell lines. Blood. 2001;98:2784–90.
doi: 10.1182/blood.V98.9.2784
Kuppers R, Hansmann ML. The Hodgkin and Reed/Sternberg cell. Int J Biochem Cell Biol. 2005;37:511–7.
doi: 10.1016/j.biocel.2003.10.025
Steidl C, Diepstra A, Lee T, Chan FC, Farinha P, Tan K, et al. Gene expression profiling of microdissected Hodgkin Reed-Sternberg cells correlates with treatment outcome in classical Hodgkin lymphoma. Blood. 2012;120:3530–40.
doi: 10.1182/blood-2012-06-439570
Delhase M, Hayakawa M, Chen Y, Karin M. Positive and negative regulation of IkappaB kinase activity through IKKbeta subunit phosphorylation. Science. 1999;284:309–13.
doi: 10.1126/science.284.5412.309
Slater SJ, Kelly MB, Taddeo FJ, Rubin E, Stubbs CD. Evidence for discrete diacylglycerol and phorbol ester activator sites on protein kinase C. Differences in effects of 1-alkanol inhibition, activation by phosphatidylethanolamine and calcium chelation. J Biol Chem. 1994;269:17160–5.
pubmed: 8006023
Zheng B, Fiumara P, Li YV, Georgakis G, Snell V, Younes M, et al. MEK/ERK pathway is aberrantly active in Hodgkin disease: a signaling pathway shared by CD30, CD40, and RANK that regulates cell proliferation and survival. Blood. 2003;102:1019–27.
doi: 10.1182/blood-2002-11-3507
Linke F, Zaunig S, Nietert MM, von Bonin F, Lutz S, Dullin C, et al. WNT5A: a motility-promoting factor in Hodgkin lymphoma. Oncogene. 2017;36:13–23.
doi: 10.1038/onc.2016.183
Anderson DM, Maraskovsky E, Billingsley WL, Dougall WC, Tometsko ME, Roux ER, et al. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature. 1997;390:175–9.
doi: 10.1038/36593
Darnay BG, Ni J, Moore PA, Aggarwal BB. Activation of NF-kappaB by RANK requires tumor necrosis factor receptor-associated factor (TRAF) 6 and NF-kappaB-inducing kinase. Identification of a novel TRAF6 interaction motif. J Biol Chem. 1999;274:7724–31.
doi: 10.1074/jbc.274.12.7724
Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004;20:781–810.
doi: 10.1146/annurev.cellbio.20.010403.113126
Kurayoshi M, Oue N, Yamamoto H, Kishida M, Inoue A, Asahara T, et al. Expression of Wnt-5a is correlated with aggressiveness of gastric cancer by stimulating cell migration and invasion. Cancer Res. 2006;66:10439–48.
doi: 10.1158/0008-5472.CAN-06-2359
Klemm F, Bleckmann A, Siam L, Chuang HN, Rietkotter E, Behme D, et al. Beta-catenin-independent WNT signaling in basal-like breast cancer and brain metastasis. Carcinogenesis. 2011;32:434–42.
doi: 10.1093/carcin/bgq269
Bakker ER, Das AM, Helvensteijn W, Franken PF, Swagemakers S, van der Valk MA, et al. Wnt5a promotes human colon cancer cell migration and invasion but does not augment intestinal tumorigenesis in Apc1638N mice. Carcinogenesis. 2013;34:2629–38.
doi: 10.1093/carcin/bgt215
Tkach V, Bock E, Berezin V. The role of RhoA in the regulation of cell morphology and motility. Cell Motil Cytoskelet. 2005;61:21–33.
doi: 10.1002/cm.20062
Larsson E, Venables PJ, Andersson AC, Fan W, Rigby S, Botling J, et al. Expression of the endogenous retrovirus ERV3 (HERV-R) during induced monocytic differentiation in the U-937 cell line. Int J Cancer. 1996;67:451–6.
doi: 10.1002/(SICI)1097-0215(19960729)67:3<451::AID-IJC23>3.0.CO;2-9
Katoh I, Mirova A, Kurata S, Murakami Y, Horikawa K, Nakakuki N, et al. Activation of the long terminal repeat of human endogenous retrovirus K by melanoma-specific transcription factor MITF-M. Neoplasia. 2011;13:1081–92.
doi: 10.1593/neo.11794
West MJ, Lowe AD, Karn J. Activation of human immunodeficiency virus transcription in T cells revisited: NF-kappaB p65 stimulates transcriptional elongation. J Virol. 2001;75:8524–37.
doi: 10.1128/JVI.75.18.8524-8537.2001
Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, et al. The NIH roadmap epigenomics mapping consortium. Nat Biotechnol. 2010;28:1045–8.
doi: 10.1038/nbt1010-1045