XRhythmic modulation of the hematopoietic niche through neutrophil clearance

María Casanova-Acebes; Christophe Pitaval; Linnea A. Weiss; César Nombela-Arrieta; Raphaël Chèvre; Noelia A-González; Yuya Kunisaki; Dachuan Zhang; Nico Van Rooijen; Leslie E. Silberstein; Christian Weber; Takashi Nagasawa; Paul S. Frenette; Antonio Castrillo; Andrés Hidalgo

doi:10.1016/j.cell.2013.04.040

XRhythmic modulation of the hematopoietic niche through neutrophil clearance

María Casanova-Acebes, Christophe Pitaval, Linnea A. Weiss, César Nombela-Arrieta, Raphaël Chèvre, Noelia A-González, Yuya Kunisaki, Dachuan Zhang, Nico Van Rooijen, Leslie E. Silberstein, Christian Weber, Takashi Nagasawa, Paul S. Frenette, Antonio Castrillo, Andrés Hidalgo

Research output: Contribution to journal › Article › peer-review

559 Scopus citations

Abstract

Unique among leukocytes, neutrophils follow daily cycles of release from and migration back into the bone marrow, where they are eliminated. Because removal of dying cells generates homeostatic signals, we explored whether neutrophil elimination triggers circadian events in the steady state. Here, we report that the homeostatic clearance of neutrophils provides cues that modulate the physiology of the bone marrow. We identify a population of CD62L ^LO CXCR4^HI neutrophils that have "aged" in the circulation and are eliminated at the end of the resting period in mice. Aged neutrophils infiltrate the bone marrow and promote reductions in the size and function of the hematopoietic niche. Modulation of the niche depends on macrophages and activation of cholesterol-sensing nuclear receptors and is essential for the rhythmic egress of hematopoietic progenitors into the circulation. Our results unveil a process that synchronizes immune and hematopoietic rhythms and expand the ascribed functions of neutrophils beyond inflammation. PaperFlick

Original language	English
Pages (from-to)	1025
Number of pages	1
Journal	Cell
Volume	153
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2013.04.040
State	Published - 23 May 2013
Externally published	Yes

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Casanova-Acebes, M., Pitaval, C., Weiss, L. A., Nombela-Arrieta, C., Chèvre, R., A-González, N., Kunisaki, Y., Zhang, D., Van Rooijen, N., Silberstein, L. E., Weber, C., Nagasawa, T., Frenette, P. S., Castrillo, A., & Hidalgo, A. (2013). XRhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell, 153(5), 1025. https://doi.org/10.1016/j.cell.2013.04.040

@article{4365d2772cfd484abc38347f01acb70c,

title = "XRhythmic modulation of the hematopoietic niche through neutrophil clearance",

abstract = "Unique among leukocytes, neutrophils follow daily cycles of release from and migration back into the bone marrow, where they are eliminated. Because removal of dying cells generates homeostatic signals, we explored whether neutrophil elimination triggers circadian events in the steady state. Here, we report that the homeostatic clearance of neutrophils provides cues that modulate the physiology of the bone marrow. We identify a population of CD62L LO CXCR4HI neutrophils that have {"}aged{"} in the circulation and are eliminated at the end of the resting period in mice. Aged neutrophils infiltrate the bone marrow and promote reductions in the size and function of the hematopoietic niche. Modulation of the niche depends on macrophages and activation of cholesterol-sensing nuclear receptors and is essential for the rhythmic egress of hematopoietic progenitors into the circulation. Our results unveil a process that synchronizes immune and hematopoietic rhythms and expand the ascribed functions of neutrophils beyond inflammation. PaperFlick",

author = "Mar{\'i}a Casanova-Acebes and Christophe Pitaval and Weiss, {Linnea A.} and C{\'e}sar Nombela-Arrieta and Rapha{\"e}l Ch{\`e}vre and Noelia A-Gonz{\'a}lez and Yuya Kunisaki and Dachuan Zhang and {Van Rooijen}, Nico and Silberstein, {Leslie E.} and Christian Weber and Takashi Nagasawa and Frenette, {Paul S.} and Antonio Castrillo and Andr{\'e}s Hidalgo",

note = "Funding Information: We thank M. N{\'a}cher, J. Ogonek, I. Ortega, V. Zorita, M. Leboeuf, J.M. Ligos, and the Cellomics, Microscopy, and Comparative Medicine Units at CNIC for technical support; J. Garaude, D. Lucas, and A. Ramiro for critically reviewing the manuscript; and S. Gonz{\'a}lez and D. Sanz for reagents. This study was supported by Deutsche Forschungsgemeinschaft (DFG WE1913/11-2 and SFB914-B8) to C.W.; R01-DK056638 and R01-HL69438 to P.S.F.; grants SAF2008-00057 and SAF2011-29244 to A.C.; Ram{\'o}n y Cajal Fellowship (RYC-2007-00697) and SAF2009-11037 from MINECO, S2010/BMD-2314 from Comunidad de Madrid, and FP7-People-IRG Program (246655) to A.H.; C.N-A. is funded by a Human Frontiers in Science Program long-term fellowship 00194/2008. M.C-A. is supported by a FPI fellowship from the Spanish Ministry of Economy and Competitivity. The Centro Nacional de Investigaciones Cardiovasculares is supported by the Spanish Ministry of Economy and Competitivity and the Pro-CNIC Foundation. M.C-A performed experiments and wrote the manuscript; L.A.W., C.P., and N.A-G performed experiments and edited the manuscript. C.N-A., R.C., Y.K., and D.Z. performed experiments; N.V.R., L.E.S., C.W., T.N., P.S.F., and A.C. contributed reagents, discussed experiments and helped in editing the manuscript; A.H. conceived the study, performed experiments and wrote the manuscript. C.P., L.A.W., and C.N-A. contributed equally to this study. ",

year = "2013",

month = may,

day = "23",

doi = "10.1016/j.cell.2013.04.040",

language = "English",

volume = "153",

pages = "1025",

journal = "Cell",

issn = "0092-8674",

publisher = "Elsevier B.V.",

number = "5",

}

Casanova-Acebes, M, Pitaval, C, Weiss, LA, Nombela-Arrieta, C, Chèvre, R, A-González, N, Kunisaki, Y, Zhang, D, Van Rooijen, N, Silberstein, LE, Weber, C, Nagasawa, T, Frenette, PS, Castrillo, A & Hidalgo, A 2013, 'XRhythmic modulation of the hematopoietic niche through neutrophil clearance', Cell, vol. 153, no. 5, pp. 1025. https://doi.org/10.1016/j.cell.2013.04.040

TY - JOUR

T1 - XRhythmic modulation of the hematopoietic niche through neutrophil clearance

AU - Casanova-Acebes, María

AU - Pitaval, Christophe

AU - Weiss, Linnea A.

AU - Nombela-Arrieta, César

AU - Chèvre, Raphaël

AU - A-González, Noelia

AU - Kunisaki, Yuya

AU - Zhang, Dachuan

AU - Van Rooijen, Nico

AU - Silberstein, Leslie E.

AU - Weber, Christian

AU - Nagasawa, Takashi

AU - Frenette, Paul S.

AU - Castrillo, Antonio

AU - Hidalgo, Andrés

N1 - Funding Information: We thank M. Nácher, J. Ogonek, I. Ortega, V. Zorita, M. Leboeuf, J.M. Ligos, and the Cellomics, Microscopy, and Comparative Medicine Units at CNIC for technical support; J. Garaude, D. Lucas, and A. Ramiro for critically reviewing the manuscript; and S. González and D. Sanz for reagents. This study was supported by Deutsche Forschungsgemeinschaft (DFG WE1913/11-2 and SFB914-B8) to C.W.; R01-DK056638 and R01-HL69438 to P.S.F.; grants SAF2008-00057 and SAF2011-29244 to A.C.; Ramón y Cajal Fellowship (RYC-2007-00697) and SAF2009-11037 from MINECO, S2010/BMD-2314 from Comunidad de Madrid, and FP7-People-IRG Program (246655) to A.H.; C.N-A. is funded by a Human Frontiers in Science Program long-term fellowship 00194/2008. M.C-A. is supported by a FPI fellowship from the Spanish Ministry of Economy and Competitivity. The Centro Nacional de Investigaciones Cardiovasculares is supported by the Spanish Ministry of Economy and Competitivity and the Pro-CNIC Foundation. M.C-A performed experiments and wrote the manuscript; L.A.W., C.P., and N.A-G performed experiments and edited the manuscript. C.N-A., R.C., Y.K., and D.Z. performed experiments; N.V.R., L.E.S., C.W., T.N., P.S.F., and A.C. contributed reagents, discussed experiments and helped in editing the manuscript; A.H. conceived the study, performed experiments and wrote the manuscript. C.P., L.A.W., and C.N-A. contributed equally to this study.

PY - 2013/5/23

Y1 - 2013/5/23

N2 - Unique among leukocytes, neutrophils follow daily cycles of release from and migration back into the bone marrow, where they are eliminated. Because removal of dying cells generates homeostatic signals, we explored whether neutrophil elimination triggers circadian events in the steady state. Here, we report that the homeostatic clearance of neutrophils provides cues that modulate the physiology of the bone marrow. We identify a population of CD62L LO CXCR4HI neutrophils that have "aged" in the circulation and are eliminated at the end of the resting period in mice. Aged neutrophils infiltrate the bone marrow and promote reductions in the size and function of the hematopoietic niche. Modulation of the niche depends on macrophages and activation of cholesterol-sensing nuclear receptors and is essential for the rhythmic egress of hematopoietic progenitors into the circulation. Our results unveil a process that synchronizes immune and hematopoietic rhythms and expand the ascribed functions of neutrophils beyond inflammation. PaperFlick

AB - Unique among leukocytes, neutrophils follow daily cycles of release from and migration back into the bone marrow, where they are eliminated. Because removal of dying cells generates homeostatic signals, we explored whether neutrophil elimination triggers circadian events in the steady state. Here, we report that the homeostatic clearance of neutrophils provides cues that modulate the physiology of the bone marrow. We identify a population of CD62L LO CXCR4HI neutrophils that have "aged" in the circulation and are eliminated at the end of the resting period in mice. Aged neutrophils infiltrate the bone marrow and promote reductions in the size and function of the hematopoietic niche. Modulation of the niche depends on macrophages and activation of cholesterol-sensing nuclear receptors and is essential for the rhythmic egress of hematopoietic progenitors into the circulation. Our results unveil a process that synchronizes immune and hematopoietic rhythms and expand the ascribed functions of neutrophils beyond inflammation. PaperFlick

UR - http://www.scopus.com/inward/record.url?scp=84878299390&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2013.04.040

DO - 10.1016/j.cell.2013.04.040

M3 - Article

C2 - 23706740

AN - SCOPUS:84878299390

SN - 0092-8674

VL - 153

SP - 1025

JO - Cell

JF - Cell

IS - 5

ER -

XRhythmic modulation of the hematopoietic niche through neutrophil clearance

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