Cell Types Promoting Goosebumps Form a Niche to Regulate Hair Follicle Stem Cells.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
06 08 2020
Historique:
received: 22 04 2019
revised: 06 04 2020
accepted: 18 06 2020
pubmed: 18 7 2020
medline: 30 3 2021
entrez: 18 7 2020
Statut: ppublish

Résumé

Piloerection (goosebumps) requires concerted actions of the hair follicle, the arrector pili muscle (APM), and the sympathetic nerve, providing a model to study interactions across epithelium, mesenchyme, and nerves. Here, we show that APMs and sympathetic nerves form a dual-component niche to modulate hair follicle stem cell (HFSC) activity. Sympathetic nerves form synapse-like structures with HFSCs and regulate HFSCs through norepinephrine, whereas APMs maintain sympathetic innervation to HFSCs. Without norepinephrine signaling, HFSCs enter deep quiescence by down-regulating the cell cycle and metabolism while up-regulating quiescence regulators Foxp1 and Fgf18. During development, HFSC progeny secretes Sonic Hedgehog (SHH) to direct the formation of this APM-sympathetic nerve niche, which in turn controls hair follicle regeneration in adults. Our results reveal a reciprocal interdependence between a regenerative tissue and its niche at different stages and demonstrate sympathetic nerves can modulate stem cells through synapse-like connections and neurotransmitters to couple tissue production with demands.

Identifiants

pubmed: 32679029
pii: S0092-8674(20)30808-4
doi: 10.1016/j.cell.2020.06.031
pmc: PMC7540726
mid: NIHMS1607799
pii:
doi:

Substances chimiques

ADRB2 protein, mouse 0
Forkhead Transcription Factors 0
Foxp1 protein, mouse 0
Hedgehog Proteins 0
Receptors, Adrenergic, beta-2 0
Repressor Proteins 0
Smo protein, mouse 0
Smoothened Receptor 0
fibroblast growth factor 18 0
Fibroblast Growth Factors 62031-54-3
Norepinephrine X4W3ENH1CV

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

578-593.e19

Subventions

Organisme : NIDDK NIH HHS
ID : P30 DK036836
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR070825
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK077097
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK102898
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2020 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests A provisional patent application has been filed by the President and Fellows of Harvard College based on this work.

Références

Acta Neuroveg (Wien). 1958;18(1-4):169-90
pubmed: 13616959
Development. 2006 Feb;133(4):581-90
pubmed: 16407399
Annu Rev Neurosci. 2016 Jul 8;39:197-216
pubmed: 27442070
Nature. 2014 May 15;509(7500):325-30
pubmed: 24828191
Elife. 2014 Feb 25;3:e01901
pubmed: 24569481
Cell Stem Cell. 2009 Sep 4;5(3):267-78
pubmed: 19664980
Nat Med. 2014 Jul;20(7):754-758
pubmed: 24952646
Cells Tissues Organs. 2016 Jun 11;201(6):423-435
pubmed: 27286967
Nucleic Acids Res. 2005 Mar 22;33(5):e51
pubmed: 15784609
Curr Biol. 1998 Sep 24;8(19):1058-68
pubmed: 9768360
Science. 2016 Feb 5;351(6273):613-7
pubmed: 26912704
Cell Rep. 2019 Apr 23;27(4):1254-1264.e7
pubmed: 31018138
Nat Med. 2018 Jun;24(6):782-791
pubmed: 29736022
Br J Dermatol. 2014 Jun;170(6):1291-8
pubmed: 24579818
Nat Med. 2014 Aug;20(8):847-56
pubmed: 25100530
Cell Rep. 2016 Mar 29;14(12):3001-18
pubmed: 27009580
Cell. 2014 May 8;157(4):935-49
pubmed: 24813615
J Invest Dermatol. 2001 Jul;117(1):3-15
pubmed: 11442744
J Neurosci. 2015 Mar 4;35(9):3893-902
pubmed: 25740518
Nature. 2014 Jun 19;510(7505):393-6
pubmed: 24870234
Dev Cell. 2015 Sep 14;34(5):577-91
pubmed: 26256211
Nature. 2019 Sep;573(7775):532-538
pubmed: 31534219
Nature. 2020 Jan;577(7792):676-681
pubmed: 31969699
Bioessays. 2005 Mar;27(3):247-61
pubmed: 15714560
Genome Biol. 2014;15(12):550
pubmed: 25516281
Elife. 2017 Feb 03;6:
pubmed: 28157072
Cell. 2001 Jan 26;104(2):233-45
pubmed: 11207364
Curr Biol. 1996 Mar 1;6(3):298-304
pubmed: 8805249
Cell Stem Cell. 2009 Feb 6;4(2):155-69
pubmed: 19200804
J Comp Neurol. 2008 Jul 10;509(2):225-38
pubmed: 18465787
Neurochem Int. 2008 Jan;52(1-2):14-25
pubmed: 17493707
Science. 2020 Jan 10;367(6474):161-166
pubmed: 31857493
Development. 2013 Sep;140(18):3809-18
pubmed: 23946441
Wiley Interdiscip Rev Dev Biol. 2017 Sep;6(5):
pubmed: 28670819
Dev Cell. 2002 May;2(5):643-53
pubmed: 12015971
J Invest Dermatol. 1999 Dec;113(6):878-87
pubmed: 10594725
Cell Rep. 2017 Nov 14;21(7):1994-2004
pubmed: 29141228
Genes Dev. 2012 Jun 1;26(11):1235-46
pubmed: 22661232
Nat Biotechnol. 2004 Apr;22(4):411-7
pubmed: 15024388
Cell Stem Cell. 2016 Aug 4;19(2):217-231
pubmed: 27320041
Mol Pain. 2011 Sep 11;7:66
pubmed: 21906401
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Immunol. 2008 Apr 1;180(7):4742-53
pubmed: 18354198
Cell. 2017 May 4;169(4):636-650.e14
pubmed: 28434617
Nat Med. 2008 Jan;14(1):64-8
pubmed: 18084302
Cell. 2011 Jan 7;144(1):92-105
pubmed: 21215372
Anat Embryol (Berl). 1995 May;191(5):407-14
pubmed: 7625611
Cell. 1994 Mar 25;76(6):1063-73
pubmed: 8137423
Dev Biol. 1999 Jan 1;205(1):1-9
pubmed: 9882493
Exp Dermatol. 1999 Aug;8(4):274-81
pubmed: 10439225
Nature. 2013 Oct 24;502(7472):513-8
pubmed: 24097351
Proc Natl Acad Sci U S A. 2016 Mar 15;113(11):E1506-15
pubmed: 26912458
Development. 2001 Dec;128(24):5099-108
pubmed: 11748145
Proc Natl Acad Sci U S A. 2018 Jul 17;115(29):E6880-E6889
pubmed: 29959210
Science. 2017 Oct 20;358(6361):321-326
pubmed: 29051371
Methods Mol Biol. 2009;482:215-32
pubmed: 19089359
Nature. 2019 Sep;573(7775):539-545
pubmed: 31534222
Pharmacol Rev. 1974 Sep;26(3):199-288
pubmed: 4376244
PLoS Genet. 2016 Jul 14;12(7):e1006150
pubmed: 27414798
Nat Commun. 2013;4:2626
pubmed: 24149709
Nat Neurosci. 2016 Oct;19(10):1331-40
pubmed: 27571008
BMC Dev Biol. 2001;1:4
pubmed: 11299042
Cell Stem Cell. 2016 Dec 1;19(6):738-751
pubmed: 27746098
J Invest Dermatol. 2012 May;132(5):1338-45
pubmed: 22297635
Physiol Meas. 2017 May;38(5):R89-R118
pubmed: 28304283
Development. 2002 Oct;129(20):4753-61
pubmed: 12361967
J Cell Biol. 2008 Dec 29;183(7):1235-42
pubmed: 19103808
Cell. 2017 Jan 12;168(1-2):295-310.e19
pubmed: 28041852
Science. 2016 Jun 17;352(6292):1471-4
pubmed: 27229141
Cell Stem Cell. 2011 Sep 2;9(3):219-32
pubmed: 21885018
Genes Dev. 2016 Oct 15;30(20):2325-2338
pubmed: 27807033
Lasers Surg Med. 2015 Jan;47(1):50-9
pubmed: 25557083
Neurosci Lett. 1993 Oct 14;161(1):105-8
pubmed: 8255535
Cell Stem Cell. 2015 Sep 3;17(3):329-40
pubmed: 26235341
Int J Trichology. 2012 Jul;4(3):154-7
pubmed: 23180923
Nat Med. 2013 Jun;19(6):695-703
pubmed: 23644514
Cell Stem Cell. 2011 May 6;8(5):552-65
pubmed: 21549329
Cell. 2001 Jun 1;105(5):599-612
pubmed: 11389830
Nat Methods. 2017 Apr;14(4):417-419
pubmed: 28263959
Nat Neurosci. 2019 Aug;22(8):1289-1305
pubmed: 31285612
Nature. 2013 Dec 12;504(7479):277-281
pubmed: 24336287
Cell. 2011 Feb 18;144(4):577-89
pubmed: 21335239
Development. 2000 Nov;127(22):4775-85
pubmed: 11044393
J Biomed Sci. 2020 Mar 14;27(1):43
pubmed: 32171310
Cell Stem Cell. 2015 Apr 2;16(4):400-12
pubmed: 25842978
Cell Rep. 2013 Jul 25;4(2):287-301
pubmed: 23850289
Cell. 2006 Jan 27;124(2):407-21
pubmed: 16439213
Nat Cell Biol. 2016 Jun;18(6):619-31
pubmed: 27183471
PLoS Genet. 2016 Jul 14;12(7):e1006151
pubmed: 27414999

Auteurs

Yulia Shwartz (Y)

Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA; Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA.

Meryem Gonzalez-Celeiro (M)

Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA; Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA; Institute of Molecular Health Sciences, ETH Zurich, 8093 Zurich, Switzerland.

Chih-Lung Chen (CL)

Department of Biomedical Engineering, College of Medicine and College of Engineering, National Taiwan University, Taipei 100, Taiwan.

H Amalia Pasolli (HA)

Electron Microscopy Resource Center, The Rockefeller University, New York, NY 10065, USA.

Shu-Hsien Sheu (SH)

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147, USA.

Sabrina Mai-Yi Fan (SM)

Department of Biomedical Engineering, College of Medicine and College of Engineering, National Taiwan University, Taipei 100, Taiwan.

Farnaz Shamsi (F)

Section on Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School, Boston, MA 02215, USA.

Steven Assaad (S)

Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA; Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA.

Edrick Tai-Yu Lin (ET)

Department of Biomedical Engineering, College of Medicine and College of Engineering, National Taiwan University, Taipei 100, Taiwan.

Bing Zhang (B)

Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA; Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA.

Pai-Chi Tsai (PC)

Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA; Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA.

Megan He (M)

Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA; Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA; Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.

Yu-Hua Tseng (YH)

Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA; Section on Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School, Boston, MA 02215, USA.

Sung-Jan Lin (SJ)

Department of Biomedical Engineering, College of Medicine and College of Engineering, National Taiwan University, Taipei 100, Taiwan; Department of Dermatology, National Taiwan University Hospital and National Taiwan University College of Medicine, Taipei 100, Taiwan; Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 100, Taiwan; Graduate Institute of Clinical Medicine, College of Medicine, National Taiwan University, Taipei 100, Taiwan. Electronic address: drsjlin@ntu.edu.tw.

Ya-Chieh Hsu (YC)

Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA; Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA. Electronic address: yachieh_hsu@harvard.edu.

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Classifications MeSH