Early acquisition of neural crest competence during hESCs neuralization

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Curchoe, Carol Lynn ^a   Maurer, Jochen ^a   Mckeown, Sonja J ^b   Cattarossi, Giulio ^a   Cimadamore, Flavio ^a   Nilbratt, Mats ^a   Snyder, Evan Y ^a   Bronner Fraser, Marianne ^b   Terskikh, Alexey V ^a  

^a BURNHAM INSTITUTE   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; CONNEXIN 43; F ACTIN; FIBRONECTIN; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR SOX10; VIMENTIN; NERVE GROWTH FACTOR RECEPTOR; PAIRED BOX TRANSCRIPTION FACTOR; PAX3 PROTEIN, HUMAN; SOX10 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; DOWN REGULATION; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MESENCHYMAL STEM CELL; NEURAL CREST CELL; NEUROEPITHELIUM; UPREGULATION; ANIMAL; CELL CULTURE; CELL MOTION; CHICK EMBRYO; CLUSTER ANALYSIS; CYTOLOGY; DNA MICROARRAY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENETICS; IMMUNOHISTOCHEMISTRY; INTESTINE; METABOLISM; MOUSE; MULTIPOTENT STEM CELL; NEURAL CREST; NEURAL STEM CELL; ORGAN CULTURE TECHNIQUE; PRENATAL DEVELOPMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

VERTEBRATA;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; CHICK EMBRYO; CLUSTER ANALYSIS; EMBRYONIC STEM CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; INTESTINES; MICE; MULTIPOTENT STEM CELLS; NEURAL CREST; NEURAL STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN CULTURE TECHNIQUES; PAIRED BOX TRANSCRIPTION FACTORS; RECEPTOR, NERVE GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOXE TRANSCRIPTION FACTORS;

EID: 78649742057     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013890     Document Type: Article

References (80)

1. 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: 737-749.
2. Wong CE, Paratore C, Dours-Zimmermann MT, Rochat A, Pietri T, et al. (2006) Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J Cell Biol 175: 1005-1015.
3. Yoshida S, Shimmura S, Nagoshi N, Fukuda K, Matsuzaki Y, et al. (2006) Isolation of multipotent neural crest-derived stem cells from the adult mouse cornea. Stem Cells 24: 2714-2722.
4. Kawaguchi J, Nichols J, Gierl MS, Faial T, Smith A (2010) Isolation and propagation of enteric neural crest progenitor cells from mouse embryonic stem cells and embryos. Development 137: 693-704.
5. LaBonne C, Bronner-Fraser M (1999) Molecular mechanisms of neural crest formation. Annu Rev Cell Dev Biol 15: 81-112.
6. LaBonne C, Bronner-Fraser M (1998) Neural crest induction in Xenopus: evidence for a two-signal model. Development 125: 2403-2414.
7. Newgreen DF, Gooday D (1985) Control of the onset of migration of neural crest cells in avian embryos. Role of Ca++-dependent cell adhesions. Cell Tissue Res 239: 329-336.
8. O'Rahilly R, Muller F (2007) The development of the neural crest in the human. J Anat 211: 335-351.
9. Yu HS (2002) Melanocyte destruction and repigmentation in vitiligo: a model for nerve cell damage and regrowth. J Biomed Sci 9: 564-573.
10. Tagra S, Talwar AK, Walia RL, Sidhu P (2006) Waardenburg syndrome. Indian J Dermatol Venereol Leprol 72: 326.
11. Marsot-Dupuch K, Smoker WR, Grauer W (2004) A rare expression of neural crest disorders: an intrasphenoidal development of the anterior pituitary gland. AJNR Am J Neuroradiol 25: 285-288.
12. Mizuseki K, Sakamoto T, Watanabe K, Muguruma K, Ikeya M, et al. (2003) Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells. Proc Natl Acad Sci U S A 100: 5828-5833.
13. Pomp O, Brokhman I, Ben-Dor I, Reubinoff BE, Goldstein RS (2005) Generation of peripheral sensory and sympathetic neurons and neural crest cells from human embryonic stem cells. Stem Cells.
14. Lazzari G, Colleoni S, Giannelli SG, Brunetti D, Colombo E, et al. (2006) Direct derivation of neural rosettes from cloned bovine blastocysts: a model of early neurulation events and neural crest specification in vitro. Stem Cells 24: 2514-2521.
15. Lee G, Kim H, Elkabetz Y, Al Shamy G, Panagiotakos G, et al. (2007) Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat Biotechnol 25: 1468-1475.
16. Jiang X, Gwye Y, McKeown SJ, Bronner-Fraser M, Lutzko C, et al. (2008) Isolation and characterization of neural crest stem cells derived from in vitro differentiated human embryonic stem cells. Stem Cells Dev.
17. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, et al. (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27: 275-280.
18. Colleoni S, Galli C, Giannelli SG, Armentero MT, Blandini F, et al. (2010) Long-term culture and differentiation of CNS precursors derived from anterior human neural rosettes following exposure to ventralizing factors. Exp Cell Res 316: 1148-1158.
19. Basch ML, Bronner-Fraser M, Garcia-Castro MI (2006) Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441: 218-222.
20. Kleber M, Lee HY, Wurdak H, Buchstaller J, Riccomagno MM, et al. (2005) Neural crest stem cell maintenance by combinatorial Wnt and BMP signaling. J Cell Biol 169: 309-320.
21. Bronner-Fraser M (2002) Molecular analysis of neural crest formation. J Physiol Paris 96: 3-8.
22. Paratore C, Goerich DE, Suter U, Wegner M, Sommer L (2001) Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128: 3949-3961.
23. Selleck MA, Garcia-Castro MI, Artinger KB, Bronner-Fraser M (1998) Effects of Shh and Noggin on neural crest formation demonstrate that BMP is required in the neural tube but not ectoderm. Development 125: 4919-4930.
24. Bajpai R, Coppola G, Kaul M, Talantova M, Cimadamore F, et al. (2009) Molecular stages of rapid and uniform neuralization of human embryonic stem cells. Cell Death Differ 16: 807-825.
25. Taneyhill LA, Bronner-Fraser M (2005) Dynamic alterations in gene expression after Wnt-mediated induction of avian neural crest. Mol Biol Cell 16: 5283-5293.
26. Rao MS, Anderson DJ (1997) Immortalization and controlled in vitro differentiation of murine multipotent neural crest stem cells. J Neurobiol 32: 722-746.
27. Maurer J, Fuchs S, Jager R, Kurz B, Sommer L, et al. (2007) Establishment and controlled differentiation of neural crest stem cell lines using conditional transgenesis. Differentiation 75: 580-591.
28. Shah NM, Groves AK, Anderson DJ (1996) Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85: 331-343.
29. Ido A, Ito K (2006) Expression of chondrogenic potential of mouse trunk neural crest cells by FGF2 treatment. Dev Dyn 235: 361-367.
30. Durbec PL, Larsson-Blomberg LB, Schuchardt A, Costantini F, Pachnis V (1996) Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development 122: 349-358.
31. Hearn CJ, Young HM, Ciampoli D, Lomax AE, Newgreen D (1999) Catenary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Dev Dyn 214: 239-247.
32. Lang D, Chen F, Milewski R, Li J, Lu MM, et al. (2000) Pax3 is required for enteric ganglia formation and functions with Sox10 to modulate expression of c-ret. J Clin Invest 106: 963-971.
33. Serbedzija GN, Bronner-Fraser M, Fraser SE (1989) A vital dye analysis of the timing and pathways of avian trunk neural crest cell migration. Development 106: 809-816.
34. Wakamatsu Y, Weston JA (1997) Sequential expression and role of Hu RNA-binding proteins during neurogenesis. Development 124: 3449-3460.
35. Elkabetz Y, Panagiotakos G, Al Shamy G, Socci ND, Tabar V, et al. (2008) Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 22: 152-165.
36. Barembaum M, Bronner-Fraser M (2005) Early steps in neural crest specification. Semin Cell Dev Biol 16: 642-646.
37. Bronner-Fraser M (2003) Hierarchy of events regulating neural crest induction. Harvey Lect 99: 129-144.
38. Henderson DJ, Copp AJ (1997) Role of the extracellular matrix in neural crest cell migration. J Anat 191(Pt 4): 507-515.
39. Wilson YM, Richards KL, Ford-Perriss ML, Panthier JJ, Murphy M (2004) Neural crest cell lineage segregation in the mouse neural tube. Development 131: 6153-6162.
40. Thomas S, Thomas M, Wincker P, Babarit C, Xu P, et al. (2008) Human neural crest cells display molecular and phenotypic hallmarks of stem cells. Hum Mol Genet 17: 3411-3425.
41. Duband JL (2006) Neural crest delamination and migration: integrating regulations of cell interactions, locomotion, survival and fate. Adv Exp Med Biol 589: 45-77.
42. Newgreen DF, Minichiello J (1996) Control of epitheliomesenchymal transformation. II. Cross-modulation of cell adhesion and cytoskeletal systems in embryonic neural cells. Dev Biol 176: 300-312.
43. Pla P, Moore R, Morali OG, Grille S, Martinozzi S, et al. (2001) Cadherins in neural crest cell development and transformation. J Cell Physiol 189: 121-132.
44. Bannerman P, Nichols W, Puhalla S, Oliver T, Berman M, et al. (2000) Early migratory rat neural crest cells express functional gap junctions: evidence that neural crest cell survival requires gap junction function. J Neurosci Res 61: 605-615.
45. Bobola N, Engist B (2008) IGFBP5 is a potential regulator of craniofacial skeletogenesis. Genesis 46: 52-59.
46. Relaix F, Rocancourt D, Mansouri A, Buckingham M (2004) Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes Dev 18: 1088-1105.
47. 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.
48. Portier MM, de Nechaud B, Gros F (1983) Peripherin, a new member of the intermediate filament protein family. Dev Neurosci 6: 335-344.
49. Anderson DJ, Groves A, Lo L, Ma Q, Rao M, et al. (1997) Cell lineage determination and the control of neuronal identity in the neural crest. Cold Spring Harb Symp Quant Biol 62: 493-504.
50. Baroffio A, Dupin E, Le Douarin NM (1988) Clone-forming ability and differentiation potential of migratory neural crest cells. Proc Natl Acad Sci U S A 85: 5325-5329.
51. Le Douarin NM, Calloni GW, Dupin E (2008) The stem cells of the neural crest. Cell Cycle 7: 1013-1019.
52. Raible DW (2006) Development of the neural crest: achieving specificity in regulatory pathways. Curr Opin Cell Biol 18: 698-703.
53. Carmona-Fontaine C, Acuna G, Ellwanger K, Niehrs C, Mayor R, (2007) Neural crests are actively precluded from the anterior neural fold by a novel inhibitory mechanism dependent on Dickkopf1 secreted by the prechordal mesoderm. Dev Biol 309: 208-221.
54. Creuzet S, Couly G, Le Douarin NM (2005) Patterning the neural crest derivatives during development of the vertebrate head: insights from avian studies. J Anat 207: 447-459.
55. Sato T, Sasai N, Sasai Y (2005) Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 132: 2355-2363.
56. 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: 4127-4138.
57. Cheung M, Briscoe J (2003) Neural crest development is regulated by the transcription factor Sox9. Development 130: 5681-5693.
58. Sander M, Paydar S, Ericson J, Briscoe J, Berber E, et al. (2000) Ventral neural patterning by Nkx homeobox genes: Nkx6.1 controls somatic motor neuron and ventral interneuron fates. Genes Dev 14: 2134-2139.
59. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF (1999) The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399: 366-370.
60. Stanke M, Junghans D, Geissen M, Goridis C, Ernsberger U, et al. (1999) The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. Development 126: 4087-4094.
61. Grillet N, Dubreuil V, Dufour HD, Brunet JF (2003) Dynamic expression of RGS4 in the developing nervous system and regulation by the neural type-specific transcription factor Phox2b. J Neurosci 23: 10613-10621.
62. Nikopoulos GN, Duarte M, Kubu CJ, Bellum S, Friesel R, et al. (2007) Soluble Jagged1 attenuates lateral inhibition, allowing for the clonal expansion of neural crest stem cells. Stem Cells 25: 3133-3142.
63. Whitlock KE, Wolf CD, Boyce ML (2003) Gonadotropin-releasing hormone (GnRH) cells arise from cranial neural crest and adenohypophyseal regions of the neural plate in the zebrafish, Danio rerio. Dev Biol 257: 140-152.
64. Whitlock KE, Smith KM, Kim H, Harden MV (2005) A role for foxd3 and sox10 in the differentiation of gonadotropin-releasing hormone (GnRH) cells in the zebrafish Danio rerio. Development 132: 5491-5502.
65. Garcia-Castro MI, Marcelle C, Bronner-Fraser M (2002) Ectodermal Wnt function as a neural crest inducer. Science 297: 848-851.
66. Anderson RB, Newgreen DF, Young HM (2006) Neural crest and the development of the enteric nervous system. Adv Exp Med Biol 589: 181-196.
67. Marchant L, Linker C, Ruiz P, Guerrero N, Mayor R (1998) The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient. Dev Biol 198: 319-329.
68. Fang D, Leishear K, Nguyen TK, Finko R, Cai K, et al. (2006) Defining the conditions for the generation of melanocytes from human embryonic stem cells. Stem Cells 24: 1668-1677.
69. Hong CS, Saint-Jeannet JP (2007) The activity of Pax3 and Zic1 regulates three distinct cell fates at the neural plate border. Mol Biol Cell 18: 2192-2202.
70. Tribulo 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: 6441-6452.
71. Monsoro-Burq AH, Wang E, Harland R (2005) Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Dev Cell 8: 167-178.
72. Meulemans D, Bronner-Fraser M (2004) Gene-regulatory interactions in neural crest evolution and development. Dev Cell 7: 291-299.
73. Sakai D, Suzuki T, Osumi N, Wakamatsu Y (2006) Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development. Development 133: 1323-1333.
74. Knecht AK, Bronner-Fraser M (2002) Induction of the neural crest: a multigene process. Nat Rev Genet 3: 453-461.
75. Burstyn-Cohen T, Stanleigh J, Sela-Donenfeld D, Kalcheim C (2004) Canonical Wnt activity regulates trunk neural crest delamination linking BMP/noggin signaling with G1/S transition. Development 131: 5327-5339.
76. Shoval I, Ludwig A, Kalcheim C (2007) Antagonistic roles of full-length N-cadherin and its soluble BMP cleavage product in neural crest delamination. Development 134: 491-501.
77. Gossrau G, Thiele J, Konang R, Schmandt T, Brustle O (2007) Bone morphogenetic protein-mediated modulation of lineage diversification during neural differentiation of embryonic stem cells. Stem Cells 25: 939-949.
78. Engler AJ, Sweeney HL, Discher DE, Schwarzbauer JE (2007) Extracellular matrix elasticity directs stem cell differentiation. J Musculoskelet Neuronal Interact 7: 335.
79. Even-Ram S, Artym V, Yamada KM (2006) Matrix control of stem cell fate. Cell 126: 645-647.
80. McKeown SJ, Newgreen DF, Farlie PG (2003) Temporal restriction of migratory and lineage potential in rhombomere 1 and 2 neural crest. Dev Biol 255: 62-76.