Daily Onset of Light and Darkness Differentially Controls Hematopoietic Stem Cell Differentiation and Maintenance

Hematopoietic stem and progenitor cells (HSPCs) tightly couple maintenance of the bone marrow (BM) reservoir, including undifferentiated long-term repopulating hematopoietic stem cells (LT-HSCs), with intensive daily production of mature leukocytes and blood replenishment. We found two daily peaks o...

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Bibliographic Details
Published in:Cell stem cell 2018-10, Vol.23 (4), p.572-585.e7
Main Authors: Golan, Karin, Kumari, Anju, Kollet, Orit, Khatib-Massalha, Eman, Subramaniam, Mohana Devi, Ferreira, Zulma S., Avemaria, Francesca, Rzeszotek, Sylwia, García-García, Andrés, Xie, Stephanie, Flores-Figueroa, Eugenia, Gur-Cohen, Shiri, Itkin, Tomer, Ludin-Tal, Aya, Massalha, Hassan, Bernshtein, Biana, Ciechanowicz, Andrzej K., Brandis, Alexander, Mehlman, Tevie, Bhattacharya, Suditi, Bertagna, Mayla, Cheng, Hui, Petrovich-Kopitman, Ekaterina, Janus, Tomasz, Kaushansky, Nathali, Cheng, Tao, Sagi, Irit, Ratajczak, Mariusz Z., Méndez-Ferrer, Simón, Dick, John E., Markus, Regina P., Lapidot, Tsvee
Format: Article
Language:English
Subjects:
Animals
bone marrow
Cell Differentiation - radiation effects
Cells, Cultured
Darkness
differentiation and egress
Epigenesis, Genetic - genetics
hematopoietic stem and progenitor cells
Hematopoietic Stem Cells - cytology
Hematopoietic Stem Cells - metabolism
Hematopoietic Stem Cells - radiation effects
Light
light and darkness
maintenance and retention
melatonin
Mice
Mice, Inbred C57BL
norepinephrine
stem cell repopulation potential
TNF
Transcription Factors - genetics
Transcription Factors - metabolism
vascular permeability
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Summary:Hematopoietic stem and progenitor cells (HSPCs) tightly couple maintenance of the bone marrow (BM) reservoir, including undifferentiated long-term repopulating hematopoietic stem cells (LT-HSCs), with intensive daily production of mature leukocytes and blood replenishment. We found two daily peaks of BM HSPC activity that are initiated by onset of light and darkness providing this coupling. Both peaks follow transient elevation of BM norepinephrine and TNF secretion, which temporarily increase HSPC reactive oxygen species (ROS) levels. Light-induced norepinephrine and TNF secretion augments HSPC differentiation and increases vascular permeability to replenish the blood. In contrast, darkness-induced TNF increases melatonin secretion to drive renewal of HSPCs and LT-HSC potential through modulating surface CD150 and c-Kit expression, increasing COX-2/αSMA+ macrophages, diminishing vascular permeability, and reducing HSPC ROS levels. These findings reveal that light- and darkness-induced daily bursts of norepinephrine, TNF, and melatonin within the BM are essential for synchronized mature blood cell production and HSPC pool repopulation. [Display omitted] •Light and dark onset induce BM NE and TNF bursts, which transiently upregulate ROS in HSPCs•NE and TNF ROS bursts induce functionally distinct 11 a.m. and 11 p.m. HSPC peaks•11 a.m. peaks of NE induce vascular permeability and HSPC differentiation and egress•11 p.m. peaks of melatonin increase CD150+ expression and HSC retention and self-renewal Golan et al. report that daily onsets of light and dark induce NE and TNF bursts that induce two different peaks of BM HSPC activity. Light-induced NE promotes HSPC differentiation and egress, replenishing mature blood cells. Dark-induced TNF promotes melatonin-dependent renewal of CD150+ HSCs and their long-term repopulation potential.
ISSN:1934-5909
1875-9777
DOI:10.1016/j.stem.2018.08.002