ArticleNature communications2019
Integrative and comparative genomic analyses identify clinically relevant pulmonary carcinoid groups and unveil the supra-carcinoids.
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Article in Nature communications, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 113 papers, 1 of them a synthesis that pooled it.
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113citing papers in PubMed, 1 pooled it
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Who cites it
113 citing papers in PubMed, 1 synthesis or guideline pooled it.
- Utility of KI-67 as a prognostic biomarker in pulmonary neuroendocrine neoplasms: a systematic review and meta-analysis.BMJ open · 2022Pooled it
- Distinct Molecular Pathways Driving Thymic and Pulmonary Neuroendocrine Neoplasms: Organ of Origin Defines Molecular Identity and Yields CD44 as a Marker of Pulmonary Neuroendocrine Tumors.Endocrine pathology · 2026Article
- VEGF pathway signalling across pulmonary neuroendocrine tumours: associations with histological subtypes in a multicentre study.Virchows Archiv : an international journal of pathology · 2026Article
- Hepatocyte nuclear factor 4 alpha defines a distinct subtype of lung carcinoid with therapeutic potential targeting somatostatin receptor 2.Virchows Archiv : an international journal of pathology · 2026Article
- Deep molecular profiling of lung neuroendocrine tumours and supra-carcinoids.Molecular cancer · 2026Article
- Mapping the path to clinical implementation of multi-omics.Nature genetics · 2026Review
- Transcriptional evidence of neuroendocrine cell plasticity beyond histological boundaries in lung neuroendocrine neoplasms: an in-silico analysis suggesting a progression model.Journal of experimental & clinical cancer research : CR · 2026Article
- Clinically actionable molecular alterations in Rb-retained small cell lung carcinoma variants.Virchows Archiv : an international journal of pathology · 2026Article
- Somatic copy number variation as a prognostic marker for recurrence in never-smokers with early-stage lung adenocarcinoma.International journal of cancer · 2026Article
- Neuroendocrine tumours through an epigenetic lens: Emerging insights for diagnosis and treatment.Journal of neuroendocrinology · 2026Review
- Three-Tier Prognostic Stratification of Lung Carcinoids (NET G1-G2-G3) by Multivariable, Data-Driven Integration of Ki-67 and Mitotic Count.Endocrine pathology · 2026Article
- Clonal relationship in a rare pulmonary mixed tumor: shared ALK fusion in atypical carcinoid and adenocarcinoma-a case report.Translational lung cancer research · 2026Article
- European Society of Neuroendocrine Tumors (ENETS) 2025 guidance paper for lung and thymic carcinoids.Journal of neuroendocrinology · 2026Article
- YAP and TEAD Are Transcriptional Regulators of Neuroendocrine Differentiation and Growth in Carcinoid Cells.The American journal of pathology · 2026Article
- Molecular alterations in high-grade neuroendocrine tumors of the small intestine.The Journal of pathology · 2026Article
- Novel concepts of cell-of origin in neuroendocrine neoplasms.Virchows Archiv : an international journal of pathology · 2026Review
- Long-term survival outcome after surgical resection of pulmonary neuroendocrine tumors.Surgery today · 2026Article
- Clinical utility of molecular profiling in rare lung neuroendocrine neoplasms.Frontiers in oncology · 2026Review
- Evidence for the transformation of a subset of pulmonary carcinoids to small cell lung carcinomas through shared molecular alterations.Frontiers in oncology · 2026Article
- Concept of neuroendocrine neoplasms of all organs with a focus on grading, subtyping.Virchows Archiv : an international journal of pathology · 2026Review
53 more citing papers are in PubMed but not listed here.
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Authors and funding
70 authors.
N AlcalaInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.ORCID http://orcid.org/0000-0002-5961-5064
N LeblayInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
A A G GabrielInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
L MangianteInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
D HervasHealth Research Institute La Fe, Avenida Fernando Abril Martorell, Torre 106 A 7planta, 46026, Valencia, Spain.
T GiffonInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.ORCID http://orcid.org/0000-0001-8133-6507
A S SertierSynergie Lyon Cancer, Centre Léon Bérard, 28 Rue Laennec, 69008, Lyon, France.
A FerrariSynergie Lyon Cancer, Centre Léon Bérard, 28 Rue Laennec, 69008, Lyon, France.
J DerksMaastricht University Medical Centre (MUMC), GROW School for Oncology and Developmental Biology, P.O. Box 5800, 6202, AZ, Maastricht, The Netherlands.ORCID http://orcid.org/0000-0002-0442-1879
A GhantousInternational Agency for Research on Cancer (IARC/WHO), Section of Mechanisms of Carcinogenesis, 150 Cours Albert Thomas, 69008, Lyon, France.
T M DelhommeInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.ORCID http://orcid.org/0000-0003-0265-4246
A ChabrierInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
C CueninInternational Agency for Research on Cancer (IARC/WHO), Section of Mechanisms of Carcinogenesis, 150 Cours Albert Thomas, 69008, Lyon, France.
B Abedi-ArdekaniInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
A BolandCentre National de Recherche en Génomique Humaine (CNRGH), Institut de Biologie François Jacob, CEA, Université Paris-Saclay, 2 rue Gaston Crémieux, CP 5706, 91057, Evry Cedex, France.
R OlasoCentre National de Recherche en Génomique Humaine (CNRGH), Institut de Biologie François Jacob, CEA, Université Paris-Saclay, 2 rue Gaston Crémieux, CP 5706, 91057, Evry Cedex, France.
V MeyerCentre National de Recherche en Génomique Humaine (CNRGH), Institut de Biologie François Jacob, CEA, Université Paris-Saclay, 2 rue Gaston Crémieux, CP 5706, 91057, Evry Cedex, France.
J AltmullerCologne Centre for Genomics (CCG) and Centre for Molecular Medicine Cologne (CMMC), University of Cologne, Weyertal 115, 50931, Cologne, Germany.
F Le Calvez-KelmInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
G DurandInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
C VoegeleInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
S BoyaultTranslational Research and Innovation Department, Cancer Genomic Platform, 28 Rue Laennec, 69008, Lyon, France.ORCID http://orcid.org/0000-0002-2297-6894
L MoonenMaastricht University Medical Centre (MUMC), GROW School for Oncology and Developmental Biology, P.O. Box 5800, 6202, AZ, Maastricht, The Netherlands.
N LemaitreInstitute for Advanced Biosciences, Site Santé, Allée des Alpes, 38700, La Tronche, Grenoble, France.
P LorimierInstitute for Advanced Biosciences, Site Santé, Allée des Alpes, 38700, La Tronche, Grenoble, France.
A C ToffartPulmonology-Physiology Unit, Grenoble Alpes University Hospital, 38700, La Tronche, France.
A SoltermannInstitute of Pathology and Molecular Pathology, University Hospital Zurich, Schmelzbergstrasse 12, 8091, Zurich, Switzerland.
J H ClementDepartment Hematology and Medical Oncology, Jena University Hospital, Am Klinikum 1, 07747, Jena, Germany.ORCID http://orcid.org/0000-0002-6601-2456
J SaengerBad Berka Institute of Pathology, Robert-Koch-Allee 9, 99438, Bad Berka, Germany.
J K FieldRoy Castle Lung Cancer Research Programme, Department of Molecular and Clinical Cancer Medicine, University of Liverpool, 6 West Derby Street, L7 8TX, Liverpool, UK.ORCID http://orcid.org/0000-0003-3951-6365
M BrevetPathology Institute, Hospices Civils de Lyon, University Claude Bernard Lyon 1, 59 Boulevard Pinel, 69677, BRON Cedex, France.ORCID http://orcid.org/0000-0003-2275-691X
C Blanc-FournierCLCC François Baclesse, 3 avenue du Général Harris, 14076, Caen Cedex 5, France.
F Galateau-SalleDepartment of Pathology, Centre Léon Bérard, 28, rue Laennec, 69373, Lyon Cedex 8, France.
N Le StangDepartment of Pathology, Centre Léon Bérard, 28, rue Laennec, 69373, Lyon Cedex 8, France.ORCID http://orcid.org/0000-0001-9522-6552
P A RussellSt. Vincent's Hospital and University of Melbourne, Victoria Parade, Fitzroy, Melbourne, VIC, 3065, Australia.
G WrightSt. Vincent's Hospital and University of Melbourne, Victoria Parade, Fitzroy, Melbourne, VIC, 3065, Australia.ORCID http://orcid.org/0000-0002-7000-9305
G SozziPathology Division Fondazione, IRCCS Istituto Nazionale dei Tumori, Via G. Venezian 1, 20133, Milan, Italy.
U PastorinoPathology Division Fondazione, IRCCS Istituto Nazionale dei Tumori, Via G. Venezian 1, 20133, Milan, Italy.
S LacommeNancy Regional University Hospital, CHRU, CRB BB-0033-00035, INSERM U1256, 29 Avenue du Maréchal de Lattre de Tassigny, 54035, Nancy Cedex, France.
J M VignaudNancy Regional University Hospital, CHRU, CRB BB-0033-00035, INSERM U1256, 29 Avenue du Maréchal de Lattre de Tassigny, 54035, Nancy Cedex, France.
V HofmanLaboratory of Clinical and Experimental Pathology, FHU OncoAge, Nice Hospital, Biobank BB-0033-00025, IRCAN Inserm U1081 CNRS 7284, University Côte d'Azur, 30 avenue de la voie Romaine, CS, 51069-06001, Nice Cedex 1, France.
P HofmanLaboratory of Clinical and Experimental Pathology, FHU OncoAge, Nice Hospital, Biobank BB-0033-00025, IRCAN Inserm U1081 CNRS 7284, University Côte d'Azur, 30 avenue de la voie Romaine, CS, 51069-06001, Nice Cedex 1, France.
O T BrustugunDrammen Hospital, Vestre Viken Health Trust, Vestre Viken HF, Postboks 800, 3004, Drammen, Norway.
M Lund-IversenInstitute of Cancer Research, Oslo University Hospital, Ullernchausseen 70, 0379, Oslo, Norway.ORCID http://orcid.org/0000-0002-2025-4062
V Thomas de MontprevilleMarie Lannelongue Hospital, 133 avenue de la Resistance, 92350, Le Plessis Robinson, France.
L A MuscarellaFondazione IRCCS Casa Sollievo della Sofferenza, Viale Cappuccini 1, 71013, San Giovanni Rotondo FG, Italy.
P GrazianoFondazione IRCCS Casa Sollievo della Sofferenza, Viale Cappuccini 1, 71013, San Giovanni Rotondo FG, Italy.ORCID http://orcid.org/0000-0001-7066-7896
H PopperDiagnostic and Research Institute of Pathology, Medical University of Graz, Neue Stiftingtalstrasse 6, 8010, Graz, Austria.ORCID http://orcid.org/0000-0003-4970-1265
J StojsicDepartment of Thoracopulmonary Pathology, Service of Pathology, Clinical Center of Serbia, Pasterova 2, Belgrade, 11000, Serbia.ORCID http://orcid.org/0000-0002-9290-0967
J F DeleuzeCentre National de Recherche en Génomique Humaine (CNRGH), Institut de Biologie François Jacob, CEA, Université Paris-Saclay, 2 rue Gaston Crémieux, CP 5706, 91057, Evry Cedex, France.
Z HercegInternational Agency for Research on Cancer (IARC/WHO), Section of Mechanisms of Carcinogenesis, 150 Cours Albert Thomas, 69008, Lyon, France.
A ViariSynergie Lyon Cancer, Centre Léon Bérard, 28 Rue Laennec, 69008, Lyon, France.
P NuernbergCologne Centre for Genomics (CCG) and Centre for Molecular Medicine Cologne (CMMC), University of Cologne, Weyertal 115, 50931, Cologne, Germany.
G PelosiDepartment of Oncology and Hemato-Oncology, University of Milan, and Inter-Hospital Pathology Division, IRCCS Multimedica, Via Gaudenzio Fantoli, 16/15, 20138, Milan, Italy.ORCID http://orcid.org/0000-0003-4725-4692
A M C DingemansMaastricht University Medical Centre (MUMC), GROW School for Oncology and Developmental Biology, P.O. Box 5800, 6202, AZ, Maastricht, The Netherlands.
M MilionePathology Division Fondazione, IRCCS Istituto Nazionale dei Tumori, Via G. Venezian 1, 20133, Milan, Italy.
L RozPathology Division Fondazione, IRCCS Istituto Nazionale dei Tumori, Via G. Venezian 1, 20133, Milan, Italy.ORCID http://orcid.org/0000-0001-5817-7149
L BrcicDiagnostic and Research Institute of Pathology, Medical University of Graz, Neue Stiftingtalstrasse 6, 8010, Graz, Austria.ORCID http://orcid.org/0000-0002-9098-8416
M VolanteDepartment of Oncology, University of Turin, Pathology Division, Via Santena 7, 10126, Torino, Italy.
M G PapottiDepartment of Oncology, University of Turin, Pathology Division, Via Santena 7, 10126, Torino, Italy.
C CauxDepartment of Immunity, Virus, and Inflammation, Cancer Research Centre of Lyon (CRCL), 28 Rue Laennec, 69008, Lyon, France.
J SandovalHealth Research Institute La Fe, Avenida Fernando Abril Martorell, Torre 106 A 7planta, 46026, Valencia, Spain.
H Hernandez-VargasCancer Research Centre of Lyon (CRCL), Inserm U 1052, CNRS UMR 5286, Centre Léon Bérard, Université de Lyon, 28 Rue Laennec, 69008, Lyon, France.ORCID http://orcid.org/0000-0001-6045-2103
E BrambillaInstitute for Advanced Biosciences, Site Santé, Allée des Alpes, 38700, La Tronche, Grenoble, France.
E J M SpeelMaastricht University Medical Centre (MUMC), GROW School for Oncology and Developmental Biology, P.O. Box 5800, 6202, AZ, Maastricht, The Netherlands.
N GirardInstitut Curie, 26 Rue d'Ulm, 75005, Paris, France.
S LantuejoulSynergie Lyon Cancer, Centre Léon Bérard, 28 Rue Laennec, 69008, Lyon, France.
J D McKayInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
M FollInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France.
L Fernandez-CuestaInternational Agency for Research on Cancer (IARC/WHO), Section of Genetics, 150 Cours Albert Thomas, 69008, Lyon, France. fernandezcuestal@iarc.fr.ORCID http://orcid.org/0000-0002-0724-6703
Funding
Genomic and transcriptomic characterization of atypical carcinoids of the lungR03CA195253 · NCI · INTERNATIONAL AGENCY FOR RES ON CANCER · PI MCKAY, JAMES DOWLING · 2015 to 2016
$113kNCI NIH HHS R03 CA195253World Health Organization 001
Abstract
The worldwide incidence of pulmonary carcinoids is increasing, but little is known about their molecular characteristics. Through machine learning and multi-omics factor analysis, we compare and contrast the genomic profiles of 116 pulmonary carcinoids (including 35 atypical), 75 large-cell neuroendocrine carcinomas (LCNEC), and 66 small-cell lung cancers. Here we report that the integrative analyses on 257 lung neuroendocrine neoplasms stratify atypical carcinoids into two prognostic groups with a 10-year overall survival of 88% and 27%, respectively. We identify therapeutically relevant molecular groups of pulmonary carcinoids, suggesting DLL3 and the immune system as candidate therapeutic targets; we confirm the value of OTP expression levels for the prognosis and diagnosis of these diseases, and we unveil the group of supra-carcinoids. This group comprises samples with carcinoid-like morphology yet the molecular and clinical features of the deadly LCNEC, further supporting the previously proposed molecular link between the low- and high-grade lung neuroendocrine neoplasms.
Indexed as
AdolescentAdultAgedAged, 80 and overBiomarkers, TumorCarcinoid TumorCarcinoma, Large CellComparative Genomic HybridizationDatasets as TopicFemaleGenomicsHomeodomain ProteinsHumansIntracellular Signaling Peptides and ProteinsLungLung NeoplasmsBiomarkers, TumorDLL3 protein, humanHomeodomain ProteinsIntracellular Signaling Peptides and ProteinsMembrane ProteinsNerve Tissue ProteinsOTP protein, human
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