Migratory patterns and evolutionary plasticity of cranial neural crest cells in ray-finned fishes.


Journal

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

Informations de publication

Date de publication:
01 11 2020
Historique:
received: 27 04 2020
revised: 13 08 2020
accepted: 14 08 2020
pubmed: 25 8 2020
medline: 11 3 2021
entrez: 25 8 2020
Statut: ppublish

Résumé

The cranial neural crest (CNC) arises within the developing central nervous system, but then migrates away from the neural tube in three consecutive streams termed mandibular, hyoid and branchial, respectively, according to the order along the anteroposterior axis. While the process of neural crest emigration generally follows a conserved anterior to posterior sequence across vertebrates, we find that ray-finned fishes (bichir, sterlet, gar, and pike) exhibit several heterochronies in the timing and order of CNC emergence that influences their subsequent migratory patterns. First, emigration of the cranial neural crest in these fishes occurs prematurely compared to other vertebrates, already initiating during early neurulation and well before neural tube closure. Second, delamination of the hyoid stream occurs prior to the more anterior mandibular stream; this is associated with early morphogenesis of key hyoid structures like external gills (bichir), a large opercular flap (gar) or first forming cartilage (pike). In sterlet, the hyoid and branchial CNC cells form a single hyobranchial sheet, which later segregates in concert with second pharyngeal pouch morphogenesis. Taken together, the results show that despite generally conserved migratory patterns, heterochronic alterations in the timing of emigration and pattern of migration of CNC cells accompanies morphological diversity of ray-finned fishes.

Identifiants

pubmed: 32835652
pii: S0012-1606(20)30228-1
doi: 10.1016/j.ydbio.2020.08.007
pmc: PMC7572781
mid: NIHMS1628478
pii:
doi:

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

14-29

Subventions

Organisme : NICHD NIH HHS
ID : P01 HD037105
Pays : United States
Organisme : NHGRI NIH HHS
ID : P50 HG004071
Pays : United States
Organisme : NIDCR NIH HHS
ID : R01 DE024157
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS111564
Pays : United States

Informations de copyright

Copyright © 2020 Elsevier Inc. All rights reserved.

Références

PLoS One. 2014 Jul 28;9(7):e102089
pubmed: 25069045
Development. 2010 Aug;137(16):2605-21
pubmed: 20663816
Development. 2002 Sep;129(18):4301-13
pubmed: 12183382
Development. 2004 Nov;131(22):5703-16
pubmed: 15509770
Dev Biol. 2018 Dec 1;444 Suppl 1:S181-S192
pubmed: 29932896
Proc Natl Acad Sci U S A. 2020 Oct 6;117(40):24876-24884
pubmed: 32958671
Nat Commun. 2019 Oct 16;10(1):4689
pubmed: 31619682
Q Rev Biol. 1983 Mar;58(1):1-28
pubmed: 6346380
Mol Phylogenet Evol. 2003 Jan;26(1):110-20
pubmed: 12470943
Dev Biol. 2018 Dec 1;444 Suppl 1:S170-S180
pubmed: 30071217
BMC Dev Biol. 2001;1:6
pubmed: 11319037
Science. 1983 Apr 15;220(4594):268-73
pubmed: 17732898
Dev Biol. 2015 Jan 15;397(2):293-304
pubmed: 25446275
Trends Genet. 2017 Oct;33(10):715-727
pubmed: 28851604
Semin Cell Dev Biol. 2010 May;21(3):325-32
pubmed: 20144910
Nature. 2017 Jul 13;547(7662):209-212
pubmed: 28678781
Nat Rev Neurosci. 2003 Oct;4(10):806-18
pubmed: 14523380
Nature. 1989 Oct 5;341(6241):405-9
pubmed: 2571936
Mech Dev. 2004 Oct;121(10):1189-97
pubmed: 15327780
Dev Biol. 2010 Aug 15;344(2):543-54
pubmed: 20399765
BMC Evol Biol. 2017 Jul 6;17(1):162
pubmed: 28683774
Zoology (Jena). 2002;105(3):195-202
pubmed: 16351868
Nat Rev Mol Cell Biol. 2008 Jul;9(7):557-68
pubmed: 18523435
J Morphol. 1992 Jul;213(1):47-83
pubmed: 29865590
Nature. 2006 May 11;441(7090):218-22
pubmed: 16688176
J Exp Zool B Mol Dev Evol. 2008 Jun 15;310(4):336-44
pubmed: 17583579
Int J Dev Biol. 1996 Aug;40(4):735-43
pubmed: 8877447
Proc Natl Acad Sci U S A. 2010 Oct 5;107(40):17262-7
pubmed: 20855630
Proc Natl Acad Sci U S A. 2018 Jun 12;115(24):6249-6254
pubmed: 29760103
Dev Biol. 2009 Aug 1;332(1):90-102
pubmed: 19433081
J Morphol. 1998 Apr;236(1):25-47
pubmed: 29852708
Development. 2003 Jun;130(11):2317-27
pubmed: 12702647
Genome Res. 2014 Feb;24(2):281-90
pubmed: 24389048
Dev Biol. 2006 Apr 1;292(1):174-88
pubmed: 16499899
Development. 1993 Feb;117(2):409-29
pubmed: 8330517
Dev Genes Evol. 2009 Jun;219(6):289-300
pubmed: 19565261
Mol Reprod Dev. 2009 Oct;76(10):954-65
pubmed: 19653285
Dev Biol. 2012 Jun 1;366(1):2-9
pubmed: 22230617
Genesis. 2018 Jun;56(6-7):e23219
pubmed: 30134069
Dev Biol. 2004 Feb 15;266(2):252-69
pubmed: 14738875
Dev Biol. 2000 Sep 15;225(2):339-56
pubmed: 10985854
Annu Rev Genet. 2018 Nov 23;52:43-63
pubmed: 30476447
Proc Natl Acad Sci U S A. 2017 Dec 12;114(50):13200-13205
pubmed: 29158384
Development. 1994 Mar;120(3):483-94
pubmed: 8162849
Elife. 2019 Mar 26;8:
pubmed: 30910008
Dev Biol. 2013 May 15;377(2):428-48
pubmed: 23473983
Dev Dyn. 1995 Jul;203(3):253-310
pubmed: 8589427
Development. 2003 Dec;130(23):5681-93
pubmed: 14522876
J Anat. 2013 Jan;222(1):79-99
pubmed: 22804777
Zoology (Jena). 2002;105(1):3-13
pubmed: 16351851
J Morphol. 2019 Aug;280(8):1118-1140
pubmed: 31188506
Nature. 2008 Dec 18;456(7224):957-61
pubmed: 19078960
PLoS One. 2015 Sep 04;10(9):e0135138
pubmed: 26339918
Genesis. 2018 Jun;56(6-7):e23107
pubmed: 29675839
Mech Dev. 2004 Jul;121(7-8):605-18
pubmed: 15210170
EMBO J. 1995 Apr 18;14(8):1697-710
pubmed: 7537662
J Exp Zool B Mol Dev Evol. 2005 Jul 15;304(4):274-97
pubmed: 16003768
Cell Adh Migr. 2010 Oct-Dec;4(4):567-85
pubmed: 20962585
Nature. 2019 Oct;574(7780):675-678
pubmed: 31645763
Dev Biol. 2004 Dec 1;276(1):225-36
pubmed: 15531376
Int J Dev Biol. 2004 Sep;48(7):663-70
pubmed: 15470639
Development. 2002 Oct;129(19):4457-68
pubmed: 12223404
PLoS One. 2008 Feb 20;3(2):e1625
pubmed: 18286182
Genome Res. 2013 Jul;23(7):1069-80
pubmed: 23817048
Proc Biol Sci. 2012 Jan 22;279(1727):224-9
pubmed: 21632625
Development. 1988;103 Suppl:121-40
pubmed: 3074905
Development. 2015 Jan 15;142(2):242-57
pubmed: 25564621
Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9360-5
pubmed: 12878728
PLoS Genet. 2018 Apr 5;14(4):e1007260
pubmed: 29621239
Rouxs Arch Dev Biol. 1993 May;202(5):250-259
pubmed: 28306037
Nature. 2015 Apr 23;520(7548):474-482
pubmed: 25903629
Dev Biol. 2012 Jun 1;366(1):34-54
pubmed: 22261150
Dev Biol. 2017 Jul 15;427(2):219-229
pubmed: 27884657
Proc Natl Acad Sci U S A. 2012 Aug 21;109(34):13698-703
pubmed: 22869754
Dev Dyn. 2019 Aug;248(8):709-727
pubmed: 30980777
J Exp Zool B Mol Dev Evol. 2007 Sep 15;308(5):591-608
pubmed: 17285635
J Anat. 2001 Jul-Aug;199(Pt 1-2):121-31
pubmed: 11523813
J Embryol Exp Morphol. 1986 Nov;98:21-58
pubmed: 3655649
Nat Commun. 2014 Dec 01;5:5661
pubmed: 25434971
Dev Dyn. 2020 Jan;249(1):88-111
pubmed: 31591788
Dev Biol. 1975 Feb;42(2):391-400
pubmed: 1167837
Wiley Interdiscip Rev Dev Biol. 2013 Jan-Feb;2(1):1-15
pubmed: 23799627
J Morphol. 1996 Jul;229(1):105-120
pubmed: 29852612
J Comp Neurol. 1998 Feb 2;391(1):99-114
pubmed: 9527545
Dev Biol. 1999 Mar 15;207(2):287-308
pubmed: 10068464
Int J Dev Biol. 1998 Jul;42(5):723-31
pubmed: 9712527
Dev Dyn. 2009 Mar;238(3):632-40
pubmed: 19235724
Mech Dev. 1997 Dec;69(1-2):3-11
pubmed: 9486527
Development. 2018 Jan 3;145(1):
pubmed: 29158447

Auteurs

Jan Stundl (J)

Department of Zoology, Faculty of Science, Charles University in Prague, Prague, Czech Republic; Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA; South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Faculty of Fisheries and Protection of Waters, University of South Bohemia in Ceske Budejovice, Vodnany, Czech Republic. Electronic address: jstundl@caltech.edu.

Anna Pospisilova (A)

Department of Zoology, Faculty of Science, Charles University in Prague, Prague, Czech Republic.

Tereza Matějková (T)

Department of Zoology, Faculty of Science, Charles University in Prague, Prague, Czech Republic.

Martin Psenicka (M)

South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Faculty of Fisheries and Protection of Waters, University of South Bohemia in Ceske Budejovice, Vodnany, Czech Republic.

Marianne E Bronner (ME)

Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA.

Robert Cerny (R)

Department of Zoology, Faculty of Science, Charles University in Prague, Prague, Czech Republic. Electronic address: robert.cerny@natur.cuni.cz.

Articles similaires

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
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH