Treatment of severe Kaposiform lymphangiomatosis positive for NRAS mutation by MEK inhibition.


Journal

Pediatric research
ISSN: 1530-0447
Titre abrégé: Pediatr Res
Pays: United States
ID NLM: 0100714

Informations de publication

Date de publication:
Dec 2023
Historique:
received: 17 08 2021
accepted: 17 01 2022
revised: 22 11 2021
pmc-release: 04 09 2023
medline: 24 11 2023
pubmed: 6 3 2022
entrez: 5 3 2022
Statut: ppublish

Résumé

Kaposiform lymphangiomatosis (KLA) is a complex lymphatic anomaly involving most commonly the mediastinum, lung, skin and bones with few effective treatments. In recent years, RAS-MAPK pathway mutations were shown to underlie the pathogenesis of several complex lymphatic anomalies. Specifically, an activating NRAS mutation (p.Q61R) was found in the majority of KLA patients. Recent reports demonstrated promising results of treatment with the MEK inhibitor, Trametinib, in patients with complex lymphatic anomalies harboring gain of function mutations in ARAF and SOS1, as well as loss of function mutation in the CBL gene, a negative regulator of the RAS-MAPK pathway. We present a 9-year-old child with a severe case of KLA harboring the typical NRAS (p.Q61R) mutation detected by plasma-derived cell free DNA, responsive to trametinib therapy. The NRAS somatic mutation was detected from plasma cfDNA using droplet digital PCR. Concurrent in-vitro studies of trametinib activity on mutant NRAS affected lymphatic endothelial cells were performed using a three-dimensional spheroid sprouting assay. Trametinib treatment lead to resolution of lifelong thrombocytopenia, improvement of pulmonary function tests and wellbeing, as well as weaning from prolonged systemic steroid treatment. Concurrent studies of mutant NRAS-expressing cells showed enhanced lymphangiogenic capacity along with over activation of the RAS-MAPK and PI3K-AKT-mTOR pathways, both reversed by trametinib. Trametinib treatment can substantially change the prognosis of patients with RAS pathway associated lymphatic anomalies. This is the first description of successful trametinib treatment of a patient with KLA harboring the most characteristic NRAS p.Q61R mutation. Treatment can significantly change the prognosis of patients with RAS pathway-associated lymphatic anomalies. We devised an in vitro model of KLA enabling a reproducible method for the continued study of disease pathogenesis. Mutated NRAS p.Q61R cells demonstrated increased lymphangiogenic capacity.

Sections du résumé

BACKGROUND BACKGROUND
Kaposiform lymphangiomatosis (KLA) is a complex lymphatic anomaly involving most commonly the mediastinum, lung, skin and bones with few effective treatments. In recent years, RAS-MAPK pathway mutations were shown to underlie the pathogenesis of several complex lymphatic anomalies. Specifically, an activating NRAS mutation (p.Q61R) was found in the majority of KLA patients. Recent reports demonstrated promising results of treatment with the MEK inhibitor, Trametinib, in patients with complex lymphatic anomalies harboring gain of function mutations in ARAF and SOS1, as well as loss of function mutation in the CBL gene, a negative regulator of the RAS-MAPK pathway. We present a 9-year-old child with a severe case of KLA harboring the typical NRAS (p.Q61R) mutation detected by plasma-derived cell free DNA, responsive to trametinib therapy.
METHODS METHODS
The NRAS somatic mutation was detected from plasma cfDNA using droplet digital PCR. Concurrent in-vitro studies of trametinib activity on mutant NRAS affected lymphatic endothelial cells were performed using a three-dimensional spheroid sprouting assay.
RESULTS RESULTS
Trametinib treatment lead to resolution of lifelong thrombocytopenia, improvement of pulmonary function tests and wellbeing, as well as weaning from prolonged systemic steroid treatment. Concurrent studies of mutant NRAS-expressing cells showed enhanced lymphangiogenic capacity along with over activation of the RAS-MAPK and PI3K-AKT-mTOR pathways, both reversed by trametinib.
CONCLUSIONS CONCLUSIONS
Trametinib treatment can substantially change the prognosis of patients with RAS pathway associated lymphatic anomalies.
IMPACT CONCLUSIONS
This is the first description of successful trametinib treatment of a patient with KLA harboring the most characteristic NRAS p.Q61R mutation. Treatment can significantly change the prognosis of patients with RAS pathway-associated lymphatic anomalies. We devised an in vitro model of KLA enabling a reproducible method for the continued study of disease pathogenesis. Mutated NRAS p.Q61R cells demonstrated increased lymphangiogenic capacity.

Identifiants

pubmed: 35246606
doi: 10.1038/s41390-022-01986-0
pii: 10.1038/s41390-022-01986-0
pmc: PMC9440952
mid: NIHMS1777482
doi:

Substances chimiques

Phosphatidylinositol 3-Kinases EC 2.7.1.-
Mitogen-Activated Protein Kinase Kinases EC 2.7.12.2
NRAS protein, human EC 3.6.1.-
Membrane Proteins 0
GTP Phosphohydrolases EC 3.6.1.-

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1911-1915

Subventions

Organisme : NCATS NIH HHS
ID : R21 TR003331
Pays : United States

Informations de copyright

© 2022. The Author(s), under exclusive licence to the International Pediatric Research Foundation, Inc.

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Auteurs

Guy Chowers (G)

Pediatrics B, Edmond and Lili Safra Children's Hospital, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel.

Gadi Abebe-Campino (G)

Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
Pediatric Hematology Oncology division, Edmond and Lily Safra Children's Hospital, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel.

Hana Golan (H)

Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
Pediatric Hematology Oncology division, Edmond and Lily Safra Children's Hospital, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel.

Asaf Vivante (A)

Pediatrics B, Edmond and Lili Safra Children's Hospital, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel.
Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
Pediatric Nephrology Unit, Edmond and Lily Safra Children's Hospital, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel.

Shoshana Greenberger (S)

Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
Pediatric Dermatology Unit, Edmond and Lily Safra Children's Hospital, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel.

Michalle Soudack (M)

Pediatric Imaging Unit, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel.

Galia Barkai (G)

Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
Pediatric Infectious Diseases Unit, Edmond and Lily Safra Children's Hospital, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel.

Ilana Fox-Fisher (I)

Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem, Israel.

Dong Li (D)

Center for Applied Genomics, The Children's Hospital of Philadelphia, Philadelphia, PA, USA.

Michael March (M)

Center for Applied Genomics, The Children's Hospital of Philadelphia, Philadelphia, PA, USA.

Mark R Battig (MR)

Center for Applied Genomics, The Children's Hospital of Philadelphia, Philadelphia, PA, USA.

Hakon Hakonarson (H)

Center for Applied Genomics, The Children's Hospital of Philadelphia, Philadelphia, PA, USA.
Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Divisions of Human Genetics and Pulmonary Medicine, The Children's Hospital of Philadelphia, Philadelphia, PA, USA.

Denise Adams (D)

Comprehensive Vascular Anomalies Program, Children's Hospital of Philadelphia, University of Pennsylvania, Philadelphia, PA, USA.

Yoav Dori (Y)

Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Jill and Mark Fishman Center for Lymphatic Disorders, The Children's Hospital of Philadelphia, Philadelphia, PA, USA.

Adi Dagan (A)

Pediatrics B, Edmond and Lili Safra Children's Hospital, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel. daganay@gmail.com.
Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel. daganay@gmail.com.
Pediatric Pulmonary Unit and the National Center for Cystic Fibrosis, Edmond and Lili Safra Children's Hospital, Chaim Sheba Medical Center at Tel Hashomer, Ramat-Gan, Israel. daganay@gmail.com.

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