Vascular Endothelial Growth Factor Receptor 3 Controls Neural Stem Cell Activation in Mice and Humans
Jinah Han,
Charles-Félix Calvo,
Tae Hyuk Kang,
Kasey L. Baker,
June-Hee Park,
Carlos Parras,
Marine Levittas,
Ulrick Birba,
Laurence Pibouin-Fragner,
Pascal Fragner,
Kaya Bilguvar,
Ronald S. Duman,
Harri Nurmi,
Kari Alitalo,
Anne C. Eichmann,
Jean-Léon Thomas
Affiliations
Jinah Han
Yale Cardiovascular Research Center, Section of Cardiovascular Medicine, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06510-3221, USA
Charles-Félix Calvo
Université Pierre and Marie Curie–Paris 6, Groupe Hospitalier Pitié-Salpètrière, 75013 Paris, France
Tae Hyuk Kang
Department of Neurology, Yale University School of Medicine, New Haven, CT 06510-3221, USA
Kasey L. Baker
Yale Cardiovascular Research Center, Section of Cardiovascular Medicine, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06510-3221, USA
June-Hee Park
Department of Neurology, Yale University School of Medicine, New Haven, CT 06510-3221, USA
Carlos Parras
Université Pierre and Marie Curie–Paris 6, Groupe Hospitalier Pitié-Salpètrière, 75013 Paris, France
Marine Levittas
Université Pierre and Marie Curie–Paris 6, Groupe Hospitalier Pitié-Salpètrière, 75013 Paris, France
Ulrick Birba
Université Pierre and Marie Curie–Paris 6, Groupe Hospitalier Pitié-Salpètrière, 75013 Paris, France
Laurence Pibouin-Fragner
Yale Cardiovascular Research Center, Section of Cardiovascular Medicine, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06510-3221, USA
Pascal Fragner
Yale Cardiovascular Research Center, Section of Cardiovascular Medicine, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06510-3221, USA
Kaya Bilguvar
Department of Genetics, Yale University School of Medicine, New Haven, CT 06510-3221, USA
Ronald S. Duman
Department of Psychiatry, Yale University School of Medicine, New Haven, CT 06510-3221, USA
Harri Nurmi
Wihuri Research Institute and Translational Cancer Biology Program, Biomedicum Helsinki, University of Helsinki, 00014 Helsinki, Finland
Kari Alitalo
Wihuri Research Institute and Translational Cancer Biology Program, Biomedicum Helsinki, University of Helsinki, 00014 Helsinki, Finland
Anne C. Eichmann
Yale Cardiovascular Research Center, Section of Cardiovascular Medicine, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06510-3221, USA
Jean-Léon Thomas
Université Pierre and Marie Curie–Paris 6, Groupe Hospitalier Pitié-Salpètrière, 75013 Paris, France
Neural stem cells (NSCs) continuously produce new neurons within the adult mammalian hippocampus. NSCs are typically quiescent but activated to self-renew or differentiate into neural progenitor cells. The molecular mechanisms of NSC activation remain poorly understood. Here, we show that adult hippocampal NSCs express vascular endothelial growth factor receptor (VEGFR) 3 and its ligand VEGF-C, which activates quiescent NSCs to enter the cell cycle and generate progenitor cells. Hippocampal NSC activation and neurogenesis are impaired by conditional deletion of Vegfr3 in NSCs. Functionally, this is associated with compromised NSC activation in response to VEGF-C and physical activity. In NSCs derived from human embryonic stem cells (hESCs), VEGF-C/VEGFR3 mediates intracellular activation of AKT and ERK pathways that control cell fate and proliferation. These findings identify VEGF-C/VEGFR3 signaling as a specific regulator of NSC activation and neurogenesis in mammals.