Conserved and context-dependent roles for pdgfrb signaling during zebrafish vascular mural cell development.

Animals Cell Differentiation Coronary Vessels / metabolism Embryonic Development Muscle, Smooth, Vascular / embryology Myocytes, Smooth Muscle / metabolism Pericytes / metabolism Proto-Oncogene Proteins c-sis / metabolism Receptor, Platelet-Derived Growth Factor beta / genetics Signal Transduction / genetics Zebrafish / embryology Zebrafish Proteins / metabolism
Mural cells Pdgfrb Pericytes Vascular smooth muscle cells Zebrafish

Journal

Developmental biology
ISSN: 1095-564X
Titre abrégé: Dev Biol
Pays: United States
ID NLM: 0372762

Informations de publication

Date de publication:
11 2021
Historique:
received: 27 05 2021
accepted: 17 06 2021
pubmed: 27 7 2021
medline: 18 11 2021
entrez: 26 7 2021
Statut: ppublish

Résumé

Platelet derived growth factor beta and its receptor, Pdgfrb, play essential roles in the development of vascular mural cells, including pericytes and vascular smooth muscle cells. To determine if this role was conserved in zebrafish, we analyzed pdgfb and pdgfrb mutant lines. Similar to mouse, pdgfb and pdgfrb mutant zebrafish lack brain pericytes and exhibit anatomically selective loss of vascular smooth muscle coverage. Despite these defects, pdgfrb mutant zebrafish did not otherwise exhibit circulatory defects at larval stages. However, beginning at juvenile stages, we observed severe cranial hemorrhage and vessel dilation associated with loss of pericytes and vascular smooth muscle cells in pdgfrb mutants. Similar to mouse, pdgfrb mutant zebrafish also displayed structural defects in the glomerulus, but normal development of hepatic stellate cells. We also noted defective mural cell investment on coronary vessels with concomitant defects in their development. Together, our studies support a conserved requirement for Pdgfrb signaling in mural cells. In addition, these zebrafish mutants provide an important model for definitive investigation of mural cells during early embryonic stages without confounding secondary effects from circulatory defects.

Identifiants

DOI: 10.1016/j.ydbio.2021.06.010 PMID: 34310924 PMC: PMC8410673
pubmed: 34310924
pii: S0012-1606(21)00152-4
doi: 10.1016/j.ydbio.2021.06.010
pmc: PMC8410673
mid: NIHMS1732327
pii:
doi:

Substances chimiques

Proto-Oncogene Proteins c-sis 0
Zebrafish Proteins 0
Receptor, Platelet-Derived Growth Factor beta EC 2.7.10.1

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

11-22

Subventions

Organisme : NHLBI NIH HHS
ID : R35 HL140017
Pays : United States
Organisme : Medical Research Council
ID : MR/J001457/1
Pays : United Kingdom

Informations de copyright

Copyright © 2021 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interest The authors declare no competing or financial interests.

Références

Genes Dev. 2003 Aug 1;17(15):1835-40
pubmed: 12897053
Cell Rep. 2017 Jan 24;18(4):1033-1047
pubmed: 28122229
Genes Dev. 1994 Aug 15;8(16):1875-87
pubmed: 7958863
Mech Dev. 2009 Aug-Sep;126(8-9):638-49
pubmed: 19539756
Nat Rev Neurol. 2018 Mar;14(3):133-150
pubmed: 29377008
J Cell Mol Med. 2015 Jan;19(1):239-48
pubmed: 25292412
Nat Genet. 2008 Mar;40(3):290-8
pubmed: 18264099
J Ultrastruct Res. 1960 Dec;4:455-72
pubmed: 13759385
Elife. 2020 Aug 24;9:
pubmed: 32831172
PLoS One. 2014 May 29;9(5):e98186
pubmed: 24873830
Dev Dyn. 2016 Jun;245(6):641-52
pubmed: 26971580
Nat Genet. 2013 Sep;45(9):1077-82
pubmed: 23913003
Dev Biol. 2007 Apr 15;304(2):735-44
pubmed: 17306248
Nature. 2018 Feb 22;554(7693):475-480
pubmed: 29443965
Dev Biol. 1996 Sep 15;178(2):375-92
pubmed: 8812136
PLoS Genet. 2020 Oct 26;16(10):e1008800
pubmed: 33104690
Nature. 2010 Nov 25;468(7323):557-61
pubmed: 20944627
Nat Commun. 2021 Apr 9;12(1):2141
pubmed: 33837218
Circ Res. 2021 Feb 19;128(4):e46-e62
pubmed: 33375813
EMBO J. 2002 Aug 15;21(16):4307-16
pubmed: 12169633
PLoS Biol. 2003 Nov;1(2):E52
pubmed: 14624252
Dev Biol. 2002 Aug 15;248(2):307-18
pubmed: 12167406
Development. 1999 Jun;126(14):3047-55
pubmed: 10375497
Development. 1998 Sep;125(17):3313-22
pubmed: 9693135
PLoS One. 2014 Mar 03;9(3):e90590
pubmed: 24594685
J Cell Biol. 2001 Apr 30;153(3):543-53
pubmed: 11331305
Dev Biol. 2014 Sep 1;393(1):10-23
pubmed: 24975012
PLoS One. 2015 Nov 23;10(11):e0143407
pubmed: 26599395
Brain. 2013 Nov;136(Pt 11):3395-407
pubmed: 24065723
J Cell Biol. 1962 Apr 1;13(1):55-87
pubmed: 19866600
Science. 1997 Jul 11;277(5323):242-5
pubmed: 9211853
Dev Dyn. 1995 Jul;203(3):253-310
pubmed: 8589427
Dev Cell. 2011 Aug 16;21(2):193-215
pubmed: 21839917
Nature. 2019 Apr;568(7751):193-197
pubmed: 30944477
Dev Cell. 2015 Jan 12;32(1):97-108
pubmed: 25533206
FASEB J. 1997 Apr;11(5):365-73
pubmed: 9141503
J Clin Invest. 2013 May;123(5):1902-10
pubmed: 23635788
J Vis Exp. 2012 Feb 23;(60):
pubmed: 22395602
Cell Rep. 2015 Jun 23;11(11):1786-96
pubmed: 26074079
Anat Embryol (Berl). 1987;176(3):373-86
pubmed: 3631536
EMBO Rep. 2019 Nov 5;20(11):e48070
pubmed: 31617312
Commun Biol. 2020 Dec 4;3(1):734
pubmed: 33277595
Gene Ther. 2008 Nov;15(21):1424-35
pubmed: 18509379
Anat Rec. 2000 Oct 1;260(2):148-57
pubmed: 10993952
Development. 2019 Jan 25;146(2):
pubmed: 30642834
Anat Rec. 2001 Sep 1;264(1):1-12
pubmed: 11505366
Development. 1998 May;125(9):1591-8
pubmed: 9521897
Brain Pathol. 2020 May;30(3):446-464
pubmed: 31561281
Hum Mutat. 2014 Aug;35(8):964-71
pubmed: 24796542
Circ Res. 2005 Sep 16;97(6):512-23
pubmed: 16166562
Nat Commun. 2020 Aug 7;11(1):3953
pubmed: 32769974
Dev Cell. 2015 May 26;33(4):442-54
pubmed: 26017769
Dev Biol. 2019 Sep 1;453(1):34-47
pubmed: 31199900
Science. 2017 Aug 25;357(6353):
pubmed: 28775214
J Exp Biol. 2002 Jun;205(Pt 12):1787-94
pubmed: 12042337
Dev Biol. 2001 Feb 15;230(2):278-301
pubmed: 11161578
Arterioscler Thromb Vasc Biol. 2009 May;29(5):630-8
pubmed: 19164813
Development. 2017 Jan 1;144(1):115-127
pubmed: 27913637
Elife. 2015 Jun 08;4:
pubmed: 26051822
Development. 2016 Apr 15;143(8):1328-39
pubmed: 26952986
FASEB J. 1987 Oct;1(4):272-81
pubmed: 3308611
Genes Dev. 1994 Aug 15;8(16):1888-96
pubmed: 7958864
Nature. 2010 Nov 25;468(7323):562-6
pubmed: 20944625
Nucleic Acids Res. 2019 Jul 2;47(W1):W171-W174
pubmed: 31106371
Genes Dev. 2008 May 15;22(10):1276-312
pubmed: 18483217
Circ Res. 2008 Dec 5;103(12):1393-401
pubmed: 18948621

Auteurs

Koji Ando (K)

Department of Immunology, Genetics and Pathology, Rudbeck Laboratory, Uppsala University, Dag Hammarskjölds Väg 20, SE-751 85, Uppsala, Sweden; Department of Molecular Pathophysiology, Institute of Advanced Medical Sciences, Nippon Medical School, Sendagi Bunkyo-ku, Tokyo, 113 8602, Japan. Electronic address: koji-ando@nms.ac.jp.

Yu-Huan Shih (YH)

Department of Molecular, Cell, and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, 01650, United States.

Lwaki Ebarasi (L)

Department of Medical Biochemistry and Biophysics, Division of Vascular Biology, Karolinska Institute, Stockholm, Sweden.

Ann Grosse (A)

Department of Molecular, Cell, and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, 01650, United States.

Daneal Portman (D)

Department of Molecular, Cell, and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, 01650, United States.

Ayano Chiba (A)

Department of Cell Biology, National Cerebral and Cardiovascular Center Research Institute, Suita, Osaka, 564 8565, Japan.

Kenny Mattonet (K)

Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Ludwigstrasse 43, 61231, Bad Nauheim, Germany.

Claudia Gerri (C)

Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Ludwigstrasse 43, 61231, Bad Nauheim, Germany; Human Embryo and Stem Cell Laboratory, The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK.

Didier Y R Stainier (DYR)

Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Ludwigstrasse 43, 61231, Bad Nauheim, Germany.

Naoki Mochizuki (N)

Department of Cell Biology, National Cerebral and Cardiovascular Center Research Institute, Suita, Osaka, 564 8565, Japan.

Shigetomo Fukuhara (S)

Department of Molecular Pathophysiology, Institute of Advanced Medical Sciences, Nippon Medical School, Sendagi Bunkyo-ku, Tokyo, 113 8602, Japan.

Christer Betsholtz (C)

Department of Immunology, Genetics and Pathology, Rudbeck Laboratory, Uppsala University, Dag Hammarskjölds Väg 20, SE-751 85, Uppsala, Sweden; Department of Medicine Huddinge (MedH), Karolinska Institutet, Campus Flemingsberg, Neo, Blickagången 16, Hiss S, Plan 7, SE-141 57, Huddinge, Sweden.

Nathan D Lawson (ND)

Department of Molecular, Cell, and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, 01650, United States. Electronic address: nathan.lawson@umassmed.edu.

Articles similaires

Evaluating the efficacy of telesurgery with dual console SSI Mantra Surgical Robotic System: experiment on animal model and clinical trials.

Sudhir Prem Srivastava, Vishwajyoti Pascual Srivastava, Avinesh Singh et al.
1.00
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell

FBXO22 inhibits colitis and colorectal carcinogenesis by regulating the degradation of the S2448-phosphorylated form of mTOR.

Minle Li, Xuan Chen, Pengfei Qu et al.
1.00
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Use of organic material provided by an automatic enrichment device by weaner pigs and its influence on tail lesions.

Philipp Heseker, Jeanette Probst, Stefanie Ammer et al.
1.00
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH

Recherchemedicale.com › Eucaryotes › Animaux › Conserved and context-dependent roles for...
Recherchemedicale.com › Phénomènes physiologiques cellulaires › Différenciation cellulaire › Conserved and context-dependent roles for...
Recherchemedicale.com › Système cardiovasculaire › Vaisseaux sanguins › Veines › Vaisseaux coronaires › Conserved and context-dependent roles for...
Recherchemedicale.com › Phénomènes physiologiques des appareils urinaire et reproducteur › Phénomènes physiologiques de la reproduction › Reproduction › Développement embryonnaire et foetal › Développement embryonnaire › Conserved and context-dependent roles for...
Recherchemedicale.com › Tissus › Muscles › Muscles lisses › Muscles lisses vasculaires › Conserved and context-dependent roles for...
Recherchemedicale.com › Cellules › Cellules musculaires › Myocytes du muscle lisse › Conserved and context-dependent roles for...
Recherchemedicale.com › Structures de l'embryon › Feuillets embryonnaires › Mésoderme › Péricytes › Conserved and context-dependent roles for...
Recherchemedicale.com › Facteurs biologiques › Protéines et peptides de signalisation intercellulaire › Facteur de croissance dérivé des plaquettes › Protéines proto-oncogènes c-sis › Conserved and context-dependent roles for...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Récepteurs peptidiques › Récepteur facteur croissance › Récepteurs aux facteurs de croissance dérivés des plaquettes › Récepteur au PDGF bêta › Conserved and context-dependent roles for...
Recherchemedicale.com › Phénomènes physiologiques cellulaires › Transduction du signal › Conserved and context-dependent roles for...
Recherchemedicale.com › Eucaryotes › Animaux › Chordés › Vertébrés › Poissons › Cypriniformes › Cyprinidae › Danio zébré › Conserved and context-dependent roles for...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines de poisson › Protéines de poisson-zèbre › Conserved and context-dependent roles for...