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Twist1 Controls a Cell-Specification Switch Governing Cell Fate Decisions within the Cardiac Neural Crest


Neural crest cells are multipotent progenitor cells that can generate both ectodermal cell types, such as neurons, and mesodermal cell types, such as smooth muscle. The mechanisms controlling this cell fate choice are not known. The basic Helix-loop-Helix (bHLH) transcription factor Twist1 is expressed throughout the migratory and post-migratory cardiac neural crest. Twist1 ablation or mutation of the Twist-box causes differentiation of ectopic neuronal cells, which molecularly resemble sympathetic ganglia, in the cardiac outflow tract. Twist1 interacts with the pro-neural factor Sox10 via its Twist-box domain and binds to the Phox2b promoter to repress transcriptional activity. Mesodermal cardiac neural crest trans-differentiation into ectodermal sympathetic ganglia-like neurons is dependent upon Phox2b function. Ectopic Twist1 expression in neural crest precursors disrupts sympathetic neurogenesis. These data demonstrate that Twist1 functions in post-migratory neural crest cells to repress pro-neural factors and thereby regulate cell fate determination between ectodermal and mesodermal lineages.


Vyšlo v časopise: Twist1 Controls a Cell-Specification Switch Governing Cell Fate Decisions within the Cardiac Neural Crest. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003405
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003405

Souhrn

Neural crest cells are multipotent progenitor cells that can generate both ectodermal cell types, such as neurons, and mesodermal cell types, such as smooth muscle. The mechanisms controlling this cell fate choice are not known. The basic Helix-loop-Helix (bHLH) transcription factor Twist1 is expressed throughout the migratory and post-migratory cardiac neural crest. Twist1 ablation or mutation of the Twist-box causes differentiation of ectopic neuronal cells, which molecularly resemble sympathetic ganglia, in the cardiac outflow tract. Twist1 interacts with the pro-neural factor Sox10 via its Twist-box domain and binds to the Phox2b promoter to repress transcriptional activity. Mesodermal cardiac neural crest trans-differentiation into ectodermal sympathetic ganglia-like neurons is dependent upon Phox2b function. Ectopic Twist1 expression in neural crest precursors disrupts sympathetic neurogenesis. These data demonstrate that Twist1 functions in post-migratory neural crest cells to repress pro-neural factors and thereby regulate cell fate determination between ectodermal and mesodermal lineages.


Zdroje

1. Bronner-FraserM (1994) Neural crest cell formation and migration in the developing embryo. FASEB Journal 8: 699–706.

2. Bronner-FraserM (1995) Origins and developmental potential of the neural crest. Experimental Cell Research 218: 405–417.

3. JainR, RentschlerS, EpsteinJA (2010) Notch and cardiac outflow tract development. Annals of the New York Academy of Sciences 1188: 184–190.

4. TrainorPA (2010) Craniofacial birth defects: The role of neural crest cells in the etiology and pathogenesis of Treacher Collins syndrome and the potential for prevention. American Journal of Medical Genetics Part A 152A: 2984–2994.

5. KirbyML, GaleTF, StewartDE (1983) Neural crest cells contribute to normal aorticopulmonary septation. Science 220: 1059–1061.

6. BrownCB, BaldwinHS (2006) Neural crest contribution to the cardiovascular system. Advances in Experimental Medicine & Biology 589: 134–154.

7. HutsonMR, KirbyML (2007) Model systems for the study of heart development and disease. Cardiac neural crest and conotruncal malformations. Seminars in Cell & Developmental Biology 18: 101–110.

8. VincentSD, BuckinghamME (2010) How to make a heart: the origin and regulation of cardiac progenitor cells. Current Topics in Developmental Biology 90: 1–41.

9. HowardMJ (2005) Mechanisms and perspectives on differentiation of autonomic neurons. Developmental Biology 277: 271–286.

10. KirbyML (1989) Plasticity and predetermination of mesencephalic and trunk neural crest transplanted into the region of the cardiac neural crest. Developmental Biology 134: 402–412.

11. WuX, HowardMJ (2001) Two signal transduction pathways involved in the catecholaminergic differentiation of avian neural crest-derived cells in vitro. Molecular & Cellular Neurosciences 18: 394–406.

12. Nelms BL, Labosky PA (2010) Transcriptional Control of Neural Crest Development. San Rafael (CA): Morgan & Claypool Life Sciences.

13. QianQ, YoungX, TaoH, ChunlinQ, JianmingX (2011) Normal and disease-related biological functions of Twist1 and underlying molecular mechanisms. Cell Research 90–116.

14. VincentzJW, BarnesRM, RodgersR, FirulliBA, ConwaySJ, et al. (2008) An Absence of Twist1 results in aberrant cardiac neural crest morphogenesis. Dev Biol 320: 131–139.

15. JiangX, IsekiS, MaxsonRE, SucovHM, Morriss-KayGM (2002) Tissue origins and interactions in the mammalian skull vault. Developmental Biology 241: 106–116.

16. BarnesRM, FirulliB, ConwaySJ, VincentzJW, FirulliAB (2010) Analysis of the Hand1 Cell Lineage Reveals Novel Contributions to Cardiovascular,Neural Crest, Extra-Embryonic, and Lateral Mesoderm Derivatives. Dev Dyn 239: 3086–3097.

17. KimJ, LoL, DormandE, AndersonDJ (2003) SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38: 17–31.

18. BiakelP, KernB, yangX, SchrockM, SosicD, et al. (2004) A Twist code determines the onset of osteoblast differentiation. Dev Cell 6: 423–435.

19. HowardM, FosterDN, CserjesiP (1999) Expression of HAND gene products may be sufficient for the differentiation of avian neural crest-derived cells into catecholaminergic neurons in culture. Developmental Biology 215: 62–77.

20. CserjesiP, BrownD, LyonsGE, OlsonEN (1995) Expression of the novel basic helix-loop-helix gene eHAND in neural crest derivatives and extraembryonic membranes during mouse development. Dev Biol 170: 664–678.

21. StankeM, JunghansD, GeissenM, GoridisC, ErnsbergerU, et al. (1999) The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. Development 126: 4087–4094.

22. StankeM, StubbuschJ, RohrerH (2004) Interaction of Mash1 and Phox2b in sympathetic neuron development. Molecular & Cellular Neurosciences 25: 374–382.

23. TsarovinaK, PattynA, StubbuschJ, MullerF, van der WeesJ, et al. (2004) Essential role of Gata transcription factors in sympathetic neuron development. Development 131: 4775–4786.

24. BurauK, StenullI, HuberK, MisawaH, BerseB, et al. (2004) c-ret regulates cholinergic properties in mouse sympathetic neurons: evidence from mutant mice. Eur J Neurosci 20: 353–362.

25. FirulliAB, McFaddenDG, LinQ, SrivastavaD, OlsonEN (1998) Heart and extra-embryonic mesodermal defects in mouse embryos lacking the bHLH transcription factor Hand1. Nature Genetics 18: 266–270.

26. HendershotTJ, LiuH, ClouthierDE, ShepherdIT, CoppolaE, et al. (2008) Conditional deletion of Hand2 reveals critical functions in neurogenesis and cell type-specific gene expression for development of neural crest-derived noradrenergic sympathetic ganglion neurons. Developmental Biology 319: 179–191.

27. FeinerL, WebberAL, BrownCB, LuMM, JiaL, et al. (2001) Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption. Development 128: 3061–3070.

28. BrownCB, FeinerL, LuMM, LiJ, MaX, et al. (2001) PlexinA2 and semaphorin signaling during cardiac neural crest development. Development 128: 3071–3080.

29. LeeMP, YutzeyKE (2011) Twist1 directly regulates genes that promote cell proliferation and migration in developing heart valves. PLoS ONE 6: e29758 doi:10.1371/journal.pone.0029758

30. SooK, O'RourkeMP, KhooP-L, SteinerKA, WongN, et al. (2002) Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Developmental Biology 247: 251–270.

31. LucasME, MullerF, RudigerR, HenionPD, RohrerH (2006) The bHLH transcription factor hand2 is essential for noradrenergic differentiation of sympathetic neurons. Development 133: 4015–4024.

32. MorikawaY, D'AutreauxF, GershonMD, CserjesiP (2007) Hand2 determines the noradrenergic phenotype in the mouse sympathetic nervous system. Developmental Biology 307: 114–126.

33. FirulliBA, KrawchukD, CentonzeVE, VirshupDE, ConwaySJ, et al. (2005) Altered Twist1 and Hand2 dimerization is associated with Saethre-Chotzen syndrome and limb abnormalities. Nat Genet 37: 373–381.

34. VincentzJW, VanDusenNJ, FlemingAB, RubartM, FirulliBA, et al. (2012) A Phox2- and Hand2-dependent Hand1 cis-regulatory element reveals a unique gene dosage requirement for Hand2 during sympathetic neurogenesis. J Neuro Sci 32: 2110–2120.

35. XuH, FirulliAB, WuX, ZhangX, HowardMJ (2003) HAND2 synergistically enhances transcription of dopamine-_B-hydroxylase in the presence of Phox2a. Dev Biol 262: 183–193.

36. HowardMJ, StankeM, SchneiderC, WuX, RohrerH (2000) The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. Development 127: 4073–4081.

37. GuS, BoyerTG, NaskiMC (2012) Basic helix-loop-helix transcription factor twist1 inhibits the transacivator function of the master chondrogenic regulator Sox9. J Biol Chem Epub ahead of print

38. WegnerM (1999) From head to toes: the multiple facets of Sox proteins. Nucleic Acids Research 27: 1409–1420.

39. FirulliBA, RedickBA, ConwaySJ, FirulliAB (2007) Mutations within helix I of Twist1 result in distinct limb defects and variation of DNA binding affinities. Journal of Biological Chemistry 282: 27536–27546.

40. ConnerneyJ, AndreevaV, LeshemY, MuentenerC, MercadoMA, et al. (2006) Twist1 dimer selection regulates cranial suture patterning and fusion. Developmental Dynamics 235: 1345–1357.

41. PaznekasWA, CunninghamML, HowardTD, KorfBR, LipsonMH, et al. (1998) Genetic heterogeneity of Saethre-Chotzen syndrome, due to TWIST and FGFR mutations. Am J Hum Genet 62: 1370–1380.

42. RoseCS, PatelP, ReardonW, MalcolmS, WinterRM (1997) The TWIST gene, although not disrupted in Saethre-Chotzen patients with apparently balanced translocations of 7p21, is mutated in familial and sporadic cases. Hum Mol Genet 6: 1369–1373.

43. HamamoriY, WuHY, SartorelliV, KedesL (1997) The basic domain of myogenic basic helix-loop-helix (bHLH) proteins is the novel target for direct inhibition by another bHLH protein, Twist. Molecular & Cellular Biology 17: 6563–6573.

44. El GhouzziV, Legeai-MalletL, Benoist-LasselinC, LajeunieE, RenierD, et al. (2001) Mutations in the basic domain and the loop-helix II junction of TWIST abolish DNA binding in Saethre-Chotzen syndrome. FEBS Lett 492: 112–118.

45. BarnesRM, FirulliAB (2009) A Twist of insight, the role of Twist-Family bHLH factors in development. Int J Dev Biol 53: 909–924.

46. PhamD, VincentzJW, FirulliAB, KaplanMH (2012) Twist1 regulates Ifng expression in Th1 cells by interfering with Runx3 function. J Immunol In press.

47. YamauchiY, AbeK, MantaniA, HitoshiY, SuzukiM, et al. (1999) A novel transgenic technique that allows specific marking of the neural crest cell lineage in mice. Developmental Biology 212: 191–203.

48. JiangX, RowitchDH, SorianoP, McMahonAP, SucovHM (2000) Fate of the mammalian cardiac neural crest. Development 127: 1607–1616.

49. PietriT, EderO, BlancheM, ThieryJP, DufourS (2003) The human tissue plasminogen activator-Cre mouse: a new tool for targeting specifically neural crest cells and their derivatives in vivo. Dev Biol 259: 176–187.

50. HildrethV, WebbS, BradshawL, BrownNA, AndersonRH, et al. (2008) Cells migrating from the neural crest contribute to the innervation of the venous pole of the heart. Journal of anatomy 212: 1–11.

51. CreazzoTL, GodtRE, LeatherburyL, ConwaySJ, KirbyML (1998) Role of cardiac neural crest cells in cardiovascular development. Annu Rev Physiol 60: 267–286.

52. MauhinV, LutzY, DennefeldC, AlbergaA (1993) Definition of the DNA-binding site repertoire for the Drosophila transcription factor SNAIL. Nucleic Acids Res 21: 3951–3957.

53. VincentT, NeveEP, JohnsonJR, KukalevA, RojoF, et al. (2009) A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol 11: 943–950.

54. Reece-HoyesJS, DeplanckeB, BarrasaMI, HatzoldJ, SmitRB, et al. (2009) The C. elegans Snail homolog CES-1 can activate gene expression in vivo and share targets with bHLH transcription factors. Nucleic Acids Res 37: 3689–3698.

55. OramKF, GridleyT (2005) Mutations in snail family genes enhance craniosynostosis of Twist1 haplo-insufficient mice: implications for Saethre-Chotzen Syndrome. Genetics 170: 971–974.

56. LeptinM (1991) Twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes & Development 5: 1568–1576.

57. CheungM, ChaboissierMC, MynettA, HirstE, SchedlA, et al. (2005) The transcriptional control of trunk neural crest induction, survival, and delamination. Developmental Cell 8: 179–192.

58. RaidR, KrinkaD, BakhoffL, AbdelwahidE, JokinenE, et al. (2009) Lack of Gata3 results in conotruncal heart anomalies in mouse. Mechanisms of Development 126: 80–89.

59. SchilhamMW, OosterwegelMA, MoererP, YaJ, de BoerPA, et al. (1996) Defects in cardiac outflow tract formation and pro-B-lymphocyte expansion in mice lacking Sox-4. Nature 380: 711–714.

60. SockE, RettigSD, EnderichJ, BoslMR, TammER, et al. (2004) Gene targeting reveals a widespread role for the high-mobility-group transcription factor Sox11 in tissue remodeling. Mol Cell Biol 24: 6635–6644.

61. PotznerMR, TsarovinaK, BinderE, Penzo-MendezA, LefebvreV, et al. (2010) Sequential requirement of Sox4 and Sox11 during development of the sympathetic nervous system. Development 137: 775–784.

62. AnsieauS, MorelAP, HinkalG, BastidJ, PuisieuxA (2010) TWISTing an embryonic transcription factor into an oncoprotein. Oncogene 29: 3173–3184.

63. YangJ, ManiSA, DonaherJL, RamaswamyS, ItzyksonRA, et al. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927–939.

64. Valsesia-WittmannS, MagdeleineM, DupasquierS, GarinE, JallasAC, et al. (2004) Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells. Cancer cell 6: 625–630.

65. WaldmannJ, SlaterEP, LangerP, BuchholzM, RamaswamyA, et al. (2009) Expression of the transcription factor snail and its target gene twist are associated with malignancy in pheochromocytomas. Annals of surgical oncology 16: 1997–2005.

66. ChenZF, Behringer (1995) Twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev 9: 686–699.

67. ChenYT, AkinwunmiPO, DengJM, TamOH, BehringerRR (2007) Generation of a Twist1 conditional null allele in the mouse. Genesis: the Journal of Genetics & Development 45: 588–592.

68. JiangX, ChoudharyB, MerkiE, ChienKR, MaxsonRE, et al. (2002) Normal fate and altered function of the cardiac neural crest cell lineage in retinoic acid receptor mutant embryos. Mechanisms of Development 117: 115–122.

69. McFaddenDG, BarbosaAC, RichardsonJA, SchneiderMD, SrivastavaD, et al. (2005) The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner. Development 132: 189–201.

70. SorianoP (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70–71.

71. PattynA, MorinX, CremerH, GoridisC, BrunetJF (1999) The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399: 366–370.

72. BarnesRM, FirulliBA, VanDusenNJ, MorikawaY, ConwaySJ, et al. (2011) Hand2 loss-of-function in Hand1-expressing cells Reveals Distinct Roles in Epicardial and Coronary Vessel Development. Circ Res 108: 940–949.

73. VincentzJW, BarnesRM, FirulliBA, ConwaySJ, FirulliAB (2008) Cooperative interaction of Nkx2.5 and Mef2c transcription factors during heart development. Developmental Dynamics 237: 3809–3819.

74. DodouE, XuSM, BlackBL (2003) mef2c is activated directly by myogenic basic helix-loop-helix proteins during skeletal muscle development in vivo. Mech Dev 120: 1021–1032.

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