Analysis of early human neural crest development
Open accessAbstract
The outstanding migration and differentiation capacities of neural crest cells (NCCs) have fascinated scientists since Wilhelm His described this cell population in 1868. Today, after intense research using vertebrate model organisms, we have gained considerable knowledge regarding the origin, migration and differentiation of NCCs. However, our understanding of NCC development in human embryos remains largely uncharacterized, despite the role the neural crest plays in several human pathologies. Here, we report for the first time the expression of a battery of molecular markers before, during, or following NCC migration in human embryos from Carnegie Stages (CS) 12 to 18. Our work demonstrates the expression of Sox9, Sox10 and Pax3 transcription factors in premigratory NCCs, while actively migrating NCCs display the additional transcription factors Pax7 and AP-2alpha. Importantly, while HNK-1 labels few migrating NCCs, p75(NTR) labels a large proportion of this population. However, the broad expression of p75(NTR) - and other markers - beyond the neural crest stresses the need for the identification of additional markers to improve our capacity to investigate human NCC development, and to enable the generation of better diagnostic and therapeutic tools.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Within the cell mass, there appeared to be two sub-types of CNCC-like cells expressing either the mesenchyme-associated marker PDGFRα or the neuro-glial-associated markers SOX10 and P75.
“Within the cell mass, there appeared to be two sub-types of CNCC-like cells expressing either the mesenchyme-associated marker PDGFRα or the neuro-glial-associated markers SOX10 and P75 (Extended Data Fig. 2)15,16.”
From Hair-bearing human skin generated entirely from pluripotent stem cells (2020) · cites this paper as [15]
The Results (Carnegie Stage 12) report SOX10- and p75NTR-positive cells in cranial mesenchyme, supporting their use as neural crest markers. The paper does not establish a PDGFRα-positive subtype or two distinct CNCC-like subtypes within the cell mass described by the citing authors. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
The citation lists haven’t been fetched yet
References 111 · Cited by 181
Research works printed but not linked: 106
- Abzhanov A Tzahor E Lassar AB Tabin CJ 2003 Dissimilar regulation of cell differentiation in mesencephalic (cranial) and sacral (trunk) neural crest cells in vitro Development 130 4567 79 12925584
- Anderson RB Stewart AL Young HM 2006 Phenotypes of neural-crest-derived cells in vagal and sacral pathways Cell Tissue Res 323 11 25 16133146
- Auerbach R 1954 Analysis of the developmental effects of a lethal mutation in the house mouse Journal of Experimental Zoology 127 305 329
- Aybar MJ Mayor R 2002 Early induction of neural crest cells: lessons learned from frog, fish and chick Curr Opin Genet Dev 12 452 8 12100892
- Bajpai R Chen DA Rada-Iglesias A Zhang J Xiong Y Helms J Chang CP Zhao Y Swigut T Wysocka J CHD7 cooperates with PBAF to control multipotent neural crest formation Nature 463 958 62 20130577 PMC2890258
- Basch ML Bronner-Fraser M Garcia-Castro MI 2006 Specification of the neural crest occurs during gastrulation and requires Pax7 Nature 441 218 22 16688176
- Benko S Fantes JA Amiel J Kleinjan DJ Thomas S Ramsay J Jamshidi N Essafi A Heaney S Gordon CT McBride D Golzio C Fisher M Perry P Abadie V Ayuso C Holder-Espinasse M Kilpatrick N Lees MM Picard A Temple IK Thomas P Vazquez MP Vekemans M Roest Crollius H Hastie ND Munnich A Etchevers HC Pelet A Farlie PG Fitzpatrick DR Lyonnet S 2009 Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence Nat Genet 41 359 64 19234473
- Beverley PC Linch D Delia D 1980 Isolation of human haematopoietic progenitor cells using monoclonal antibodies Nature 287 332 3 7421991
- Bi W Huang W Whitworth DJ Deng JM Zhang Z Behringer RR de Crombrugghe B 2001 Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization Proc Natl Acad Sci U S A 98 6698 703 11371614 PMC34415
- Bixby S Kruger GM Mosher JT Joseph NM Morrison SJ 2002 Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity Neuron 35 643 56 12194865
- Bondurand N Dastot-Le Moal F Stanchina L Collot N Baral V Marlin S Attie-Bitach T Giurgea I Skopinski L Reardon W Toutain A Sarda P Echaieb A Lackmy-Port-Lis M Touraine R Amiel J Goossens M Pingault V 2007 Deletions at the SOX10 gene locus cause Waardenburg syndrome types 2 and 4 Am J Hum Genet 81 1169 85 17999358 PMC2276340
- Bondurand N Kobetz A Pingault V Lemort N Encha-Razavi F Couly G Goerich DE Wegner M Abitbol M Goossens M 1998 Expression of the SOX10 gene during human development FEBS Lett 432 168 72 9720918
- Brokhman I Gamarnik-Ziegler L Pomp O Aharonowiz M Reubinoff BE Goldstein RS 2008 Peripheral sensory neurons differentiate from neural precursors derived from human embryonic stem cells Differentiation 76 145 55 17608731
- Bronner-Fraser M 1986 Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1 Dev Biol 115 44 55 3516760
- Cheng Y Cheung M Abu-Elmagd MM Orme A Scotting PJ 2000 Chick sox10, a transcription factor expressed in both early neural crest cells and central nervous system Brain Res Dev Brain Res 121 233 41 10876038
- Cheung M Briscoe J 2003 Neural crest development is regulated by the transcription factor Sox9 Development 130 5681 93 14522876
- Conway SJ Henderson DJ Kirby ML Anderson RH Copp AJ 1997 Development of a lethal congenital heart defect in the splotch (Pax3) mutant mouse Cardiovasc Res 36 163 73 9463628
- Couly GF Le Douarin NM 1987 Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds: implications for the genesis of cephalic human congenital abnormalities Dev Biol 120 198 214 3817289
- Creazzo TL Godt RE Leatherbury L Conway SJ Kirby ML 1998 Role of cardiac neural crest cells in cardiovascular development Annu Rev Physiol 60 267 86 9558464
- Dottori M Gross MK Labosky P Goulding M 2001 The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate Development 128 4127 38 11684651
- Dutton KA Pauliny A Lopes SS Elworthy S Carney TJ Rauch J Geisler R Haffter P Kelsh RN 2001 Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates Development 128 4113 25 11684650
- Etchevers HC Amiel J Lyonnet S 2006 Molecular bases of human neurocristopathies Adv Exp Med Biol 589 213 34 17076285
- Farlie PG McKeown SJ Newgreen DF 2004 The neural crest: basic biology and clinical relationships in the craniofacial and enteric nervous systems Birth Defects Res C Embryo Today 72 173 89 15269891
- Foerst-Potts L Sadler TW 1997 Disruption of Msx-1 and Msx-2 reveals roles for these genes in craniofacial, eye, and axial development Dev Dyn 209 70 84 9142497
- Fougerousse F Durand M Lopez S Suel L Demignon J Thornton C Ozaki H Kawakami K Barbet P Beckmann JS Maire P 2002 Six and Eya expression during human somitogenesis and MyoD gene family activation J Muscle Res Cell Motil 23 255 64 12500905
- Galli LM Knight SR Barnes TL Doak AK Kadzik RS Burrus LW 2008 Identification and characterization of subpopulations of Pax3 and Pax7 expressing cells in developing chick somites and limb buds Dev Dyn 237 1862 74 18521946 PMC2854025
- Gérard M Abitbol M Delezoide AL Dufier JL Mallet J Vekemans M 1995 PAX-genes expression during human embryonic development, a preliminary report C R Acad Sci III 318 57 66 7757805
- Gershon TR Oppenheimer O Chin SS Gerald WL 2005 Temporally regulated neural crest transcription factors distinguish neuroectodermal tumors of varying malignancy and differentiation Neoplasia 7 575 84 16036108 PMC1501286
- Gomperts M Garcia-Castro M Wylie C Heasman J 1994 Interactions between primordial germ cells play a role in their migration in mouse embryos Development 120 135 41 8119122
- Goulding M Lumsden A Paquette AJ 1994 Regulation of Pax-3 expression in the dermomyotome and its role in muscle development Development 120 957 71 7600971
- Goulding MD Chalepakis G Deutsch U Erselius JR Gruss P 1991 Pax-3, a novel murine DNA binding protein expressed during early neurogenesis EMBO J 10 1135 47 2022185 PMC452767
- Hammond CL Hinits Y Osborn DP Minchin JE Tettamanti G Hughes SM 2007 Signals and myogenic regulatory factors restrict pax3 and pax7 expression to dermomyotome-like tissue in zebrafish Dev Biol 302 504 21 17094960 PMC3960072
- Hanley NA Hagan DM Clement-Jones M Ball SG Strachan T Salas-Cortes L McElreavey K Lindsay S Robson S Bullen P Ostrer H Wilson DI 2000 SRY, SOX9, and DAX1 expression patterns during human sex determination and gonadal development Mech Dev 91 403 7 10704874
- Hill RE Jones PF Rees AR Sime CM Justice MJ Copeland NG Jenkins NA Graham E Davidson DR 1989 A new family of mouse homeo box-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1 Genes Dev 3 26 37 2565278
- Hoth CF Milunsky A Lipsky N Sheffer R Clarren SK Baldwin CT 1993 Mutations in the paired domain of the human PAX3 gene cause Klein-Waardenburg syndrome (WS-III) as well as Waardenburg syndrome type I (WS-I) Am J Hum Genet 52 455 62 8447316 PMC1682157
- Houzelstein D Cheraud Y Auda-Boucher G Fontaine-Perus J Robert B 2000 The expression of the homeobox gene Msx1 reveals two populations of dermal progenitor cells originating from the somites Development 127 2155 64 10769239
- Ishii M Han J Yen HY Sucov HM Chai Y Maxson RE Jr 2005 Combined deficiencies of Msx1 and Msx2 cause impaired patterning and survival of the cranial neural crest Development 132 4937 50 16221730
- Jakobsen LP Ullmann R Christensen SB Jensen KE Molsted K Henriksen KF Hansen C Knudsen MA Larsen LA Tommerup N Tumer Z 2007 Pierre Robin sequence may be caused by dysregulation of SOX9 and KCNJ2 J Med Genet 44 381 6 17551083 PMC2740883
- Jiang X Gwye Y McKeown SJ Bronner-Fraser M Lutzko C Lawlor ER 2009 Isolation and characterization of neural crest stem cells derived from in vitro-differentiated human embryonic stem cells Stem Cells Dev 18 1059 70 19099373 PMC4606969
- Josephson A Widenfalk J Trifunovski A Widmer HR Olson L Spenger C 2001 GDNF and NGF family members and receptors in human fetal and adult spinal cord and dorsal root ganglia J Comp Neurol 440 204 17 11745618
- Jostes B Walther C Gruss P 1990 The murine paired box gene, Pax7, is expressed specifically during the development of the nervous and muscular system Mech Dev 33 27 37 1982921
- Kaufman MH 1992 The Atlas of Mouse Development Academic Press London
- Kent J Wheatley SC Andrews JE Sinclair AH Koopman P 1996 A male-specific role for SOX9 in vertebrate sex determination Development 122 2813 22 8787755
- Kuhlbrodt K Herbarth B Sock E Hermans-Borgmeyer I Wegner M 1998 Sox10, a novel transcriptional modulator in glial cells J Neurosci 18 237 50 9412504 PMC6793382
- Lacosta AM Muniesa P Ruberte J Sarasa M Dominguez L 2005 Novel expression patterns of Pax3/Pax7 in early trunk neural crest and its melanocyte and non-melanocyte lineages in amniote embryos Pigment Cell Res 18 243 51 16029418
- Lallemand Y Nicola MA Ramos C Bach A Cloment CS Robert B 2005 Analysis of Msx1; Msx2 double mutants reveals multiple roles for Msx genes in limb development Development 132 3003 14 15930102
- Lane PW Liu HM 1984 Association of megacolon with a new dominant spotting gene (Dom) in the mouse J Hered 75 435 9 6512238
- Lang D Powell SK Plummer RS Young KP Ruggeri BA 2007 PAX genes: roles in development, pathophysiology, and cancer Biochem Pharmacol 73 1 14 16904651
- Lee G Kim H Elkabetz Y Al Shamy G Panagiotakos G Barberi T Tabar V Studer L 2007 Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells Nat Biotechnol 25 1468 75 18037878
- Li M Zhao C Wang Y Zhao Z Meng A 2002 Zebrafish sox9b is an early neural crest marker Dev Genes Evol 212 203 6 12012235
- Li W Cornell RA 2007 Redundant activities of Tfap2a and Tfap2c are required for neural crest induction and development of other non-neural ectoderm derivatives in zebrafish embryos Dev Biol 304 338 54 17258188 PMC1904501
- Lumsden A Sprawson N Graham A 1991 Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo Development 113 1281 91 1811942
- MacKenzie A Ferguson MW Sharpe PT 1992 Expression patterns of the homeobox gene, Hox-8, in the mouse embryo suggest a role in specifying tooth initiation and shape Development 115 403 20 1358591
- Mansouri A Stoykova A Torres M Gruss P 1996 Dysgenesis of cephalic neural crest derivatives in Pax7−/− mutant mice Development 122 831 8 8631261
- Mayor R Young R Vargas A 1999 Development of neural crest in Xenopus Curr Top Dev Biol 43 85 113 9891884
- McKeown SJ Lee VM Bronner-Fraser M Newgreen DF Farlie PG 2005 Sox10 overexpression induces neural crest-like cells from all dorsoventral levels of the neural tube but inhibits differentiation Dev Dyn 233 430 44 15768395
- Meulemans D Bronner-Fraser M 2004 Gene-regulatory interactions in neural crest evolution and development Dev Cell 7 291 9 15363405
- Milunsky JM Maher TA Zhao G Roberts AE Stalker HJ Zori RT Burch MN Clemens M Mulliken JB Smith R Lin AE 2008 TFAP2A mutations result in branchio-oculo-facial syndrome Am J Hum Genet 82 1171 7 18423521 PMC2427243
- Minchin JE Hughes SM 2008 Sequential actions of Pax3 and Pax7 drive xanthophore development in zebrafish neural crest Dev Biol 317 508 22 18417109 PMC3005709
- Mitchell PJ Timmons PM Hebert JM Rigby PW Tjian R 1991 Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis Genes Dev 5 105 19 1989904
- Mori-Akiyama Y Akiyama H Rowitch DH de Crombrugghe B 2003 Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest Proc Natl Acad Sci U S A 100 9360 5 12878728 PMC170923
- Morrison SJ White PM Zock C Anderson DJ 1999 Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells Cell 96 737 49 10089888
- Müller F O'Rahilly R 1984 Cerebral dysraphia (future anencephaly) in a human twin embryo at stage 13 Teratology 30 167 77 6388010
- Müller F O'Rahilly R 1986 The development of the human brain and the closure of the rostral neuropore at stage 11 Anat Embryol (Berl) 175 205 22 3826651
- Müller F O'Rahilly R 1987 The development of the human brain, the closure of the caudal neuropore, and the beginning of secondary neurulation at stage 12 Anat Embryol (Berl) 176 413 30 3688450
- Müller F O'Rahilly R 1991 Development of anencephaly and its variants Am J Anat 190 193 218 2048550
- Muratovska A Zhou C He S Goodyer P Eccles MR 2003 Paired-Box genes are frequently expressed in cancer and often required for cancer cell survival Oncogene 22 7989 97 12970747
- Ng LJ Wheatley S Muscat GE Conway-Campbell J Bowles J Wright E Bell DM Tam PP Cheah KS Koopman P 1997 SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse Dev Biol 183 108 21 9119111
- Nichols DH 1981 Neural crest formation in the head of the mouse embryo as observed using a new histological technique J Embryol Exp Morphol 64 105 20 7031165
- Noden DM 1975 An analysis of migratory behavior of avian cephalic neural crest cells Dev Biol 42 106 30 1112437
- O'Rahilly R Müller F 2007 The development of the neural crest in the human J Anat 211 335 51 17848161 PMC2375817
- Otto A Schmidt C Patel K 2006 Pax3 and Pax7 expression and regulation in the avian embryo Anat Embryol (Berl) 211 293 310 16506066
- Patthey C Edlund T Gunhaga L 2009 Wnt-regulated temporal control of BMP exposure directs the choice between neural plate border and epidermal fate Development 136 73 83 19060333
- Patthey C Gunhaga L Edlund T 2008 Early development of the central and peripheral nervous systems is coordinated by Wnt and BMP signals PLoS One 3 e1625 18286182 PMC2229838
- Pingault V Ente D Dastot-Le Moal F Goossens M Marlin S Bondurand N Review and update of mutations causing Waardenburg syndrome Hum Mutat 31 391 406 20127975
- Pomp O Brokhman I Ben-Dor I Reubinoff B Goldstein RS 2005 Generation of peripheral sensory and sympathetic neurons and neural crest cells from human embryonic stem cells Stem Cells 23 923 30 15883233
- Pusch C Hustert E Pfeifer D Sudbeck P Kist R Roe B Wang Z Balling R Blin N Scherer G 1998 The SOX10/Sox10 gene from human and mouse: sequence, expression, and transactivation by the encoded HMG domain transcription factor Hum Genet 103 115 23 9760192
- Raible DW Wood A Hodsdon W Henion PD Weston JA Eisen JS 1992 Segregation and early dispersal of neural crest cells in the embryonic zebrafish Dev Dyn 195 29 42 1292751
- Robert B Sassoon D Jacq B Gehring W Buckingham M 1989 Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis EMBO J 8 91 100 2565810 PMC400776
- Sarnat HB Flores-Sarnat L 2005 Embryology of the neural crest: its inductive role in the neurocutaneous syndromes J Child Neurol 20 637 43 16225807
- Sauka-Spengler T Bronner-Fraser M 2008 A gene regulatory network orchestrates neural crest formation Nat Rev Mol Cell Biol 9 557 68 18523435
- Scholl FA Kamarashev J Murmann OV Geertsen R Dummer R Schafer BW 2001 PAX3 is expressed in human melanomas and contributes to tumor cell survival Cancer Res 61 823 6 11221862
- Serbedzija GN Bronner-Fraser M Fraser SE 1992 Vital dye analysis of cranial neural crest cell migration in the mouse embryo Development 116 297 307 1283734
- Serbedzija GN Fraser SE Bronner-Fraser M 1990 Pathways of trunk neural crest cell migration in the mouse embryo as revealed by vital dye labelling Development 108 605 12 2387238
- Shen H Wilke T Ashique AM Narvey M Zerucha T Savino E Williams T Richman JM 1997 Chicken transcription factor AP-2: cloning, expression and its role in outgrowth of facial prominences and limb buds Dev Biol 188 248 66 9268573
- Sieber-Blum M 1989 SSEA-1 is a specific marker for the spinal sensory neuron lineage in the quail embryo and in neural crest cell cultures Dev Biol 134 362 75 2568298
- Southard-Smith EM Kos L Pavan WJ 1998 Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model Nat Genet 18 60 4 9425902
- Steventon B Carmona-Fontaine C Mayor R 2005 Genetic network during neural crest induction: from cell specification to cell survival Semin Cell Dev Biol 16 647 54 16084743
- Sull JW Sull JW Liang K-Y Hetmanski JB Fallin MD Ingersoll RG Park J Wu-Chou Y-H Chen PK Chong SS Cheah F Yeow V Park BY Jee SH Jabs EW Redett R Scott AF Beaty TH 2009 Maternal transmission effects of the PAX genes among cleft case-parent trios from four populations Eur J Hum Genet 17 831 839 19142206 PMC2760446
- Suzuki T Sakai D Osumi N Wada H Wakamatsu Y 2006 Sox genes regulate type 2 collagen expression in avian neural crest cells Dev Growth Differ 48 477 86 17026712
- Tam PK Garcia-Barceló M 2009 Genetic basis of Hirschsprung's disease Pediatr Surg Int 25 543 58 19521704
- Terzić J Saraga-Babić M 1999 Expression pattern of PAX3 and PAX6 genes during human embryogenesis Int J Dev Biol 43 501 8 10610023
- Thomas S Thomas M Wincker P Babarit C Xu P Speer MC Munnich A Lyonnet S Vekemans M Etchevers HC 2008 Human neural crest cells display molecular and phenotypic hallmarks of stem cells Hum Mol Genet 17 3411 25 18689800 PMC2566525
- Tremblay P Dietrich S Mericskay M Schubert FR Li Z Paulin D 1998 A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors Dev Biol 203 49 61 9806772
- Tremblay P Kessel M Gruss P 1995 A transgenic neuroanatomical marker identifies cranial neural crest deficiencies associated with the Pax3 mutant Splotch Dev Biol 171 317 29 7556916
- Tríbulo C Aybar MJ Nguyen VH Mullins MC Mayor R 2003 Regulation of Msx genes by a Bmp gradient is essential for neural crest specification Development 130 6441 52 14627721
- Tucker GC Aoyama H Lipinski M Tursz T Thiery JP 1984 Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes Cell Differ 14 223 30 6207939
- Tucker GC Delarue M Zada S Boucaut JC Thiery JP 1988 Expression of the HNK-1/NC-1 epitope in early vertebrate neurogenesis Cell Tissue Res 251 457 65 2449968
- van den Boogaard MJ Dorland M Beemer FA van Amstel HK 2000 MSX1 mutation is associated with orofacial clefting and tooth agenesis in humans Nat Genet 24 342 3 10742093
- Velagaleti GV Bien-Willner GA Northup JK Lockhart LH Hawkins JC Jalal SM Withers M Lupski JR Stankiewicz P 2005 Position effects due to chromosome breakpoints that map approximately 900 Kb upstream and approximately 1.3 Mb downstream of SOX9 in two patients with campomelic dysplasia Am J Hum Genet 76 652 62 15726498 PMC1199302
- von Schack D Casademunt E Schweigreiter R Meyer M Bibel M Dechant G 2001 Complete ablation of the neurotrophin receptor p75NTR causes defects both in the nervous and the vascular system Nat Neurosci 4 977 8 11559852
- Wagner T Wirth J Meyer J Zabel B Held M Zimmer J Pasantes J Bricarelli FD Keutel J Hustert E 1994 Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9 Cell 79 1111 20 8001137
- Wilson YM Richards KL Ford-Perriss ML Panthier JJ Murphy M 2004 Neural crest cell lineage segregation in the mouse neural tube Development 131 6153 62 15548576
- Yokouchi Y Ohsugi K Sasaki H Kuroiwa A 1991 Chicken homeobox gene Msx-1: structure, expression in limb buds and effect of retinoic acid Development 113 431 44 1685987
- Zhang J Hagopian-Donaldson S Serbedzija G Elsemore J Plehn-Dujowich D McMahon AP Flavell RA Williams T 1996 Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2 Nature 381 238 41 8622766
- Zhao Q Eberspaecher H Lefebvre V De Crombrugghe B 1997 Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis Dev Dyn 209 377 86 9264261
- Authors
- Betters, E., Liu, Y., Kjaeldgaard, A., Sundström, E., & García-Castro, M. I.
- Affiliations
- Yale University (US)
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2010-08
- Volume
- 344
- Issue
- 2
- Pages
- 578-592
- ISSN
- 0012-1606 (ISSN-L)
- PMC
- PMC2927129
- OpenAlex
- W2091048750
- Cited by
- 181
- References
- 111
- Citations by year
- 2026: 6 · 2025: 9 · 2024: 7 · 2023: 8 · 2022: 12 · 2021: 16 · 2020: 15 · 2019: 12 · 2018: 11 · 2017: 13 · 2016: 14 · 2015: 9 · 2014: 11 · 2013: 17 · 2012: 13
- FWCI
- 4.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1117 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Swedish Research Council
- Stockholm's Sjukhem Foundation
- Knut och Alice Wallenberg Foundation
- Yale University
- Yale University Developmental Biology Training Grant
- NIH
- State of Conecticut (RO1DE017914, 09SCAYALE45)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Surgery › Congenital gastrointestinal and neural anomalies
- Keywords
- neural crest cells, human embryo, neural crest migration, neural crest differentiation, molecular markers, SOX9, SOX10, Pax3, Pax7, AP-2α, HNK-1, p75 neurotrophin receptor, transcription factors
- MeSH terms
- Cell Differentiation, Humans, Neural Crest, Neurons, Transcription Factors, PAX7 Transcription Factor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review