Transforming growth factor β-mediated sox10 suppression controls mesenchymal progenitor generation in neural crest stem cells

Stem Cells

Volumn 29, Issue 4, 2011, Pages 689-699

  John, Nessy ^a,b   Cinelli, Paolo ^a   Wegner, Michael ^c   Sommer, Lukas ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Mesenchymal progenitors; Neural crest stem cell; Sox10; TGF

Indexed keywords

TRANSCRIPTION FACTOR SOX10; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL CYCLE REGULATION; CELL FATE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE INACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MORPHOGENESIS; MOUSE; MULTIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NEURAL CREST CELL; NEURAL STEM CELL; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; REGENERATIVE MEDICINE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MORPHOGENESIS; NEURAL CREST; PERIPHERAL NERVOUS SYSTEM; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOXE TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

VERTEBRATA;

EID: 79953776015     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.607     Document Type: Article

References (37)

1. Le Douarin NM, Creuzet S, Couly G, et al. Neural crest cell plasticity and its limits. Development (Cambridge, England) 2004;131: 4637-4650. (Pubitemid 39433452)
2. Calloni GW, Glavieux-Pardanaud C, Le Douarin NM, et al. Sonic Hedgehog promotes the development of multipotent neural crest progenitors endowed with both mesenchymal and neural potentials. Proc Natl Acad Sci USA 2007;104:19879-19884.
3. Calloni GW, Le Douarin NM, Dupin E. High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities. Proc Natl Acad Sci USA 2009; 106:8947-8952.
4. Lwigale PY, Conrad GW, Bronner-Fraser M. Graded potential of neural crest to form cornea, sensory neurons and cartilage along the rostrocaudal axis. Development (Cambridge, England) 2004;131:1979-1991. (Pubitemid 38702033)
5. Ido A, Ito K. Expression of chondrogenic potential of mouse trunk neural crest cells by FGF2 treatment. Dev Dyn 2006;235:361-367. (Pubitemid 43100942)
6. McGonnell IM, Graham A. Trunk neural crest has skeletogenic potential. Curr Biol 2002;12:767-771. (Pubitemid 34455433)
7. Takashima Y, Era T, Nakao K, et al. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 2007;129:1377-1388. (Pubitemid 46970707)
8. Wurdak H, Ittner LM, Sommer L. DiGeorge syndrome and pharyngeal apparatus development. Bioessays 2006;28:1078-1086. (Pubitemid 44714117)
9. Chai Y, Ito Y, Han J. TGF-beta signaling and its functional significance in regulating the fate of cranial neural crest cells. Crit Rev Oral Biol Med 2003;14:78-88.
10. Wurdak H, Ittner LM, Lang KS, et al. Inactivation of TGFbeta signaling in neural crest stem cells leads to multiple defects reminiscent of DiGeorge syndrome. Genes Dev 2005;19:530-535. (Pubitemid 40314985)
11. Loeys BL, Chen J, Neptune ER, et al. A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat Genet 2005;37:275-281. (Pubitemid 41716254)
12. Danielian PS, Muccino D, Rowitch DH, et al. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 1998;8:1323-1326. (Pubitemid 29006707)
13. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999;21:70-71. (Pubitemid 29036285)
14. Britsch S, Goerich DE, Riethmacher D, et al. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 2001;15:66-78. (Pubitemid 32060683)
15. Hari L, Brault V, Kleber M, et al. Lineage-specific requirements of beta-catenin in neural crest development. J Cell Biol 2002;159: 867-880. (Pubitemid 36008368)
16. Paratore C, Goerich DE, Suter U, et al. Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development (Cambridge, England) 2001;128:3949-3961. (Pubitemid 33040603)
17. Stemple DL, Anderson DJ. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 1992;71:973-985.
18. Akiyama H, Chaboissier MC, Behringer RR, et al. Essential role of Sox9 in the pathway that controls formation of cardiac valves and septa. Proc Natl Acad Sci USA 2004;101:6502-6507. (Pubitemid 38586003)
19. Mori-Akiyama Y, Akiyama H, Rowitch DH, et al. Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proc Natl Acad Sci USA 2003;100:9360-9365. (Pubitemid 37033933)
20. Furumatsu T, Tsuda M, Taniguchi N, et al. Smad3 induces chondrogenesis through the activation of SOX9 via CREB-binding protein/ p300 recruitment. J Biol Chem 2005;280:8343-8350. (Pubitemid 40349737)
21. Shah NM, Groves AK, Anderson DJ. Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 1996;85:331-343. (Pubitemid 26160705)
22. Akiyama H, Kim JE, Nakashima K, et al. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci USA 2005;102:14665-14670. (Pubitemid 41457113)
23. Nakashima K, Zhou X, Kunkel G, et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002;108:17-29. (Pubitemid 34137009)
24. Sommer L, Shah N, Rao M, et al. The cellular function of MASH1 in autonomic neurogenesis. Neuron 1995;15:1245-1258.
25. Abzhanov A, Tabin CJ. Shh and Fgf8 act synergistically to drive cartilage outgrowth during cranial development. Dev Biol 2004;273:134-148. (Pubitemid 39078372)
26. Vitelli F, Zhang Z, Huynh T, et al. Fgf8 expression in the Tbx1 domain causes skeletal abnormalities and modifies the aortic arch but not the out- flow tract phenotype of Tbx1 mutants. Dev Biol 2006;295:559-570. (Pubitemid 43927694)
27. Bixby S, Kruger GM, Mosher JT, et al. Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron 2002;35:643-656. (Pubitemid 35223025)
28. Fuchs S, Herzog D, Sumara G, et al. Stage-specific control of neural crest stem cell proliferation by the small rho GTPases Cdc42 and Rac1. Cell Stem cell 2009;4:236-247.
29. Falk S, Wurdak H, Ittner LM, et al. Brain area-specific effect of TGFbeta signaling on Wnt-dependent neural stem cell expansion. Cell Stem cell 2008;2:472-483. (Pubitemid 351598080)
30. Buchmann-Moller S, Miescher I, John N, et al. Multiple lineage-specific roles of Smad4 during neural crest development. Dev Biol 2009; 330:329-338.
31. Kim J, Lo L, Dormand E, et al. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 2003;38:17-31. (Pubitemid 36423350)
32. Paratore C, Eichenberger C, Suter U, et al. Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease. Hum Mol Genet 2002;11:3075-3085. (Pubitemid 35414821)
33. Dupin E, Calloni GW, Le Douarin NM. The cephalic neural crest of amniote vertebrates is composed of a large majority of precursors endowed with neural, melanocytic, chondrogenic and osteogenic potentialities. Cell cycle (Georgetown, TX) 2010;9: 238-249.
34. Finzsch M, Stolt CC, Lommes P, et al. Sox9 and Sox10 influence survival and migration of oligodendrocyte precursors in the spinal cord by regulating PDGF receptor alpha expression. Development (Cambridge, England) 2008;135:637-646. (Pubitemid 351405017)
35. Taylor KM, Labonne C. SoxE factors function equivalently during neural crest and inner ear development and their activity is regulated by SUMOylation. Dev Cell 2005;9:593-603. (Pubitemid 41555142)
36. Chimal-Monroy J, Rodriguez-Leon J, Montero JA, et al. Analysis of the molecular cascade responsible for mesodermal limb chondrogenesis: Sox genes and BMP signaling. Dev Biol 2003;257: 292-301. (Pubitemid 36506845)
37. Dutton KA, Pauliny A, Lopes SS, et al. Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development (Cambridge, England) 2001;128:4113-4125. (Pubitemid 33077026)