Epigenomics and Single-Cell Sequencing Define a Developmental Hierarchy in Langerhans Cell Histiocytosis.


Journal

Cancer discovery
ISSN: 2159-8290
Titre abrégé: Cancer Discov
Pays: United States
ID NLM: 101561693

Informations de publication

Date de publication:
10 2019
Historique:
received: 01 02 2019
revised: 03 06 2019
accepted: 10 07 2019
pubmed: 28 7 2019
medline: 13 8 2020
entrez: 27 7 2019
Statut: ppublish

Résumé

Langerhans cell histiocytosis (LCH) is a rare neoplasm predominantly affecting children. It occupies a hybrid position between cancers and inflammatory diseases, which makes it an attractive model for studying cancer development. To explore the molecular mechanisms underlying the pathophysiology of LCH and its characteristic clinical heterogeneity, we investigated the transcriptomic and epigenomic diversity in primary LCH lesions. Using single-cell RNA sequencing, we identified multiple recurrent types of LCH cells within these biopsies, including putative LCH progenitor cells and several subsets of differentiated LCH cells. We confirmed the presence of proliferative LCH cells in all analyzed biopsies using IHC, and we defined an epigenomic and gene-regulatory basis of the different LCH-cell subsets by chromatin-accessibility profiling. In summary, our single-cell analysis of LCH uncovered an unexpected degree of cellular, transcriptomic, and epigenomic heterogeneity among LCH cells, indicative of complex developmental hierarchies in LCH lesions. SIGNIFICANCE: This study sketches a molecular portrait of LCH lesions by combining single-cell transcriptomics with epigenome profiling. We uncovered extensive cellular heterogeneity, explained in part by an intrinsic developmental hierarchy of LCH cells. Our findings provide new insights and hypotheses for advancing LCH research and a starting point for personalizing therapy.

Identifiants

pubmed: 31345789
pii: 2159-8290.CD-19-0138
doi: 10.1158/2159-8290.CD-19-0138
pmc: PMC6795548
mid: EMS84423
doi:

Substances chimiques

Biomarkers 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1406-1421

Subventions

Organisme : European Research Council
ID : 679146
Pays : International
Organisme : Austrian Science Fund FWF
ID : F 6102
Pays : Austria

Commentaires et corrections

Type : CommentIn

Informations de copyright

©2019 American Association for Cancer Research.

Références

Adv Immunol. 2013;120:127-61
pubmed: 24070383
PLoS Med. 2007 Aug;4(8):e253
pubmed: 17696642
J Immunol. 2010 Apr 15;184(8):4557-67
pubmed: 20220088
Bioinformatics. 2012 Mar 15;28(6):882-3
pubmed: 22257669
Cell. 2004 Aug 20;118(4):409-18
pubmed: 15315754
J Mol Diagn. 2007 Jul;9(3):337-44
pubmed: 17591933
Hematology Am Soc Hematol Educ Program. 2015;2015:559-64
pubmed: 26637772
Bioinformatics. 2011 Apr 1;27(7):1017-8
pubmed: 21330290
Trends Immunol. 2017 Nov;38(11):817-828
pubmed: 28720426
Blood. 2017 Jul 13;130(2):176-180
pubmed: 28566492
BMC Bioinformatics. 2013 Apr 15;14:128
pubmed: 23586463
Blood. 2012 Dec 20;120(26):5199-208
pubmed: 23074278
Blood. 2014 Nov 6;124(19):3007-15
pubmed: 25202140
Nature. 2017 Sep 21;549(7672):389-393
pubmed: 28854169
Genome Biol. 2014;15(12):550
pubmed: 25516281
BMC Bioinformatics. 2014 Jun 12;15:182
pubmed: 24925680
Nat Immunol. 2017 Aug;18(8):877-888
pubmed: 28650480
Science. 2017 Apr 21;356(6335):
pubmed: 28428369
Bioinformatics. 2016 Feb 15;32(4):587-9
pubmed: 26508757
Cancer Discov. 2016 Feb;6(2):154-65
pubmed: 26566875
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
Virchows Arch. 2013 Feb;462(2):219-28
pubmed: 23269323
Pediatr Blood Cancer. 2017 Mar;64(3):
pubmed: 27663873
Cell. 2006 Apr 21;125(2):315-26
pubmed: 16630819
Dis Model Mech. 2009 Sep-Oct;2(9-10):436-9
pubmed: 19726802
Cell Death Dis. 2017 Jun 22;8(6):e2895
pubmed: 28640249
Pediatr Res. 2019 May;85(6):856-864
pubmed: 30474648
Lancet. 1994 Mar 26;343(8900):767-8
pubmed: 7510816
Cell. 2016 Nov 17;167(5):1369-1384.e19
pubmed: 27863249
Nucleic Acids Res. 2017 Apr 20;45(7):e54
pubmed: 27998929
Immunity. 2016 Sep 20;45(3):626-640
pubmed: 27637148
Nat Commun. 2017 Jun 01;8:15599
pubmed: 28569836
Nat Biotechnol. 2018 Jun;36(5):411-420
pubmed: 29608179
Nat Rev Cancer. 2016 Dec;16(12):759-773
pubmed: 27687979
Eur J Immunol. 2008 Nov;38(11):2975-80
pubmed: 18991275
Cell Commun Signal. 2015 Feb 22;13:13
pubmed: 25889448
Nucleic Acids Res. 2018 Jan 4;46(D1):D252-D259
pubmed: 29140464
Nat Methods. 2013 Dec;10(12):1213-8
pubmed: 24097267
Eur J Immunol. 2014 Feb;44(2):553-60
pubmed: 24165969
Semin Cell Dev Biol. 2015 May;41:30-8
pubmed: 24613914
J Pathol. 2006 Aug;209(4):474-83
pubmed: 16718746
Genome Biol. 2008;9(9):R137
pubmed: 18798982
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Blood. 2008 Oct 15;112(8):3186-93
pubmed: 18641369
Commun Biol. 2019 Aug 9;2:306
pubmed: 31428694
Brief Bioinform. 2018 Oct 5;:null
pubmed: 30289442
Blood. 2017 Jul 13;130(2):167-175
pubmed: 28512190
J Exp Med. 2016 Apr 4;213(4):585-603
pubmed: 27001747
Oncogene. 2016 Apr 7;35(14):1770-84
pubmed: 26119944
Sci Rep. 2013 Oct 24;3:3039
pubmed: 24154593
Nature. 2006 May 18;441(7091):349-53
pubmed: 16625203
Nat Methods. 2017 Oct;14(10):959-962
pubmed: 28846090
Am J Cancer Res. 2015 Mar 15;5(4):1542-52
pubmed: 26101717
Nat Rev Immunol. 2013 Jul;13(7):499-509
pubmed: 23787991
Blood. 2016 Jun 2;127(22):2672-81
pubmed: 26966089
Lancet Oncol. 2017 Feb;18(2):e113-e125
pubmed: 28214412
N Engl J Med. 2018 Aug 30;379(9):856-868
pubmed: 30157397
N Engl J Med. 1994 Jul 21;331(3):154-60
pubmed: 8008029
Mol Cell Biol. 2001 Jul;21(13):4330-6
pubmed: 11390661

Auteurs

Florian Halbritter (F)

CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria.
St. Anna Children's Cancer Research Institute (CCRI), Vienna, Austria.

Matthias Farlik (M)

CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria.
Department of Dermatology, Medical University of Vienna, Vienna, Austria.

Raphaela Schwentner (R)

St. Anna Children's Cancer Research Institute (CCRI), Vienna, Austria.

Gunhild Jug (G)

St. Anna Children's Cancer Research Institute (CCRI), Vienna, Austria.

Nikolaus Fortelny (N)

CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria.

Thomas Schnöller (T)

St. Anna Children's Cancer Research Institute (CCRI), Vienna, Austria.

Hanja Pisa (H)

St. Anna Children's Cancer Research Institute (CCRI), Vienna, Austria.

Linda C Schuster (LC)

CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria.

Andrea Reinprecht (A)

Department of Neurosurgery, Medical University of Vienna, Vienna, Austria.

Thomas Czech (T)

Department of Neurosurgery, Medical University of Vienna, Vienna, Austria.

Johannes Gojo (J)

Department of Pediatrics, Medical University of Vienna, Vienna, Austria.

Wolfgang Holter (W)

St. Anna Children's Cancer Research Institute (CCRI), Vienna, Austria.
Department of Pediatrics, Medical University of Vienna, Vienna, Austria.
St. Anna Children's Hospital, St. Anna Kinderspital, Vienna, Austria.

Milen Minkov (M)

St. Anna Children's Cancer Research Institute (CCRI), Vienna, Austria.
Department of Pediatrics, Adolescent Medicine and Neonatology, Rudolfstiftung Hospital, Vienna, Austria.

Wolfgang M Bauer (WM)

Department of Dermatology, Medical University of Vienna, Vienna, Austria.

Ingrid Simonitsch-Klupp (I)

Clinical Institute of Pathology, Medical University of Vienna, Vienna, Austria.

Christoph Bock (C)

CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria. caroline.hutter@stanna.at cbock@cemm.oeaw.ac.at.
Department of Laboratory Medicine, Medical University of Vienna, Vienna, Austria.
Max Planck Institute for Informatics, Saarland Informatics Campus, Saarbrücken, Germany.
Ludwig Boltzmann Institute for Rare and Undiagnosed Diseases, Vienna, Austria.

Caroline Hutter (C)

St. Anna Children's Cancer Research Institute (CCRI), Vienna, Austria. caroline.hutter@stanna.at cbock@cemm.oeaw.ac.at.
Department of Pediatrics, Medical University of Vienna, Vienna, Austria.
St. Anna Children's Hospital, St. Anna Kinderspital, Vienna, Austria.

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Classifications MeSH