Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development

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How individual cell fates are specified from multipotent progenitor cells is a fundamental question in developmental and stem cell biology. Accumulating evidence indicates that stem cells develop into each of their final, diverse cell-types after progression through one or more partially-restricted intermediates, but the molecular mechanisms underlying final fate choice are largely unknown. Neural crest cells (NCCs) give rise to diverse cell-types including multiple pigment cells and thus are a favored model for understanding the mechanism of fate specification. We have investigated how a specific fate choice is made from partially-restricted pigment cell progenitors in medaka. We show that Sry-related transcription factor Sox5 is required for fate determination between yellow xanthophore and white leucophore, and its loss causes excessive formation of leucophores and absence of xanthophores. We demonstrate that Sox5 functions cell-autonomously in the xanthophore lineage in medaka. Furthermore, pax7a is expressed in the partially-restricted progenitor cells shared with xanthophore and leucophore lineages, and Sox5 acts in some of these cells to promote xanthophore lineage. Our work reveals the role of Sox5 as a molecular switch determining xanthophore versus leucophore fate choice from the shared progenitor, and identifies an important mechanism regulating pigment cell fate choice from NCCs.

Vyšlo v časopise: Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004246
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004246

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Zdroje

1. DonoghuePC, GrahamA, KelshRN (2008) The origin and evolution of the neural crest. Bioessays 30: 530–541.

2. Le DouarinNM, CreuzetS, CoulyG, DupinE (2004) Neural crest cell plasticity and its limits. Development 131: 4637–4650.

3. FujiiR (1993) Cytophysiology of fish chromatophores. Int Rev Cytol 143: 191–255.

4. KelshRN (2004) Genetics and evolution of pigment patterns in fish. Pigment Cell Res 17: 326–336.

5. KelshRN, BrandM, JiangYJ, HeisenbergCP, LinS, et al. (1996) Zebrafish pigmentation mutations and the processes of neural crest development. Development 123: 369–389.

6. OdiorneJM (1933) The Occurrence of Guanophores in Fundulus. Proc Natl Acad Sci U S A 19: 750–754.

7. FriesEF (1942) White Pigmentary Effectors (Leucophores) in Killifishes. Proc Natl Acad Sci U S A 28: 396–401.

8. TakeuchiIK (1976) Electron microscopy of two types of reflecting chromatophores (iridophores and leucophores) in the guppy, Lebistes reticulatus Peters. Cell Tissue Res 173: 17–27.

9. Hama T (1975) In: Yamamoto T, editor. Medaka (KILLFISH): Biology and Strains. Tokyo: Keigaku Publishing Company. pp. 138–153.

10. OliphantLW, HudonJ (1993) Pteridines as reflecting pigments and components of reflecting organelles in vertebrates. Pigment Cell Res 6: 205–208.

11. BraaschI, SchartlM, VolffJN (2007) Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol Biol 7: 74.

12. Le DouarinNM, DupinE (2003) Multipotentiality of the neural crest. Curr Opin Genet Dev 13: 529–536.

13. CalloniGW, Glavieux-PardanaudC, Le DouarinNM, DupinE (2007) Sonic Hedgehog promotes the development of multipotent neural crest progenitors endowed with both mesenchymal and neural potentials. Proc Natl Acad Sci U S A 104: 19879–19884.

14. CalloniGW, Le DouarinNM, DupinE (2009) High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities. Proc Natl Acad Sci U S A 106: 8947–8952.

15. BhattS, DiazR, TrainorPA (2013) Signals and switches in Mammalian neural crest cell differentiation. Cold Spring Harb Perspect Biol 5 (2) pii: a008326. doi: 10.1101

16. TassabehjiM, NewtonVE, ReadAP (1994) Waardenburg syndrome type 2 caused by mutations in the human microphthalmia (MITF) gene. Nat Genet 8: 251–255.

17. MochiiM, MazakiY, MizunoN, HayashiH, EguchiG (1998) Role of Mitf in differentiation and transdifferentiation of chicken pigmented epithelial cell. Dev Biol 193: 47–62.

18. ListerJA, RobertsonCP, LepageT, JohnsonSL, RaibleDW (1999) nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126: 3757–3767.

19. HodgkinsonCA, MooreKJ, NakayamaA, SteingrimssonE, CopelandNG, et al. (1993) Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix-zipper protein. Cell 74: 395–404.

20. LeeM, GoodallJ, VerasteguiC, BallottiR, GodingCR (2000) Direct regulation of the Microphthalmia promoter by Sox10 links Waardenburg-Shah syndrome (WS4)-associated hypopigmentation and deafness to WS2. J Biol Chem 275: 37978–37983.

21. ElworthyS, ListerJA, CarneyTJ, RaibleDW, KelshRN (2003) Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 130: 2809–2818.

22. BondurandN, PingaultV, GoerichDE, LemortN, SockE, et al. (2000) Interaction among SOX10, PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum Mol Genet 9: 1907–1917.

23. LacostaAM, MuniesaP, RuberteJ, SarasaM, DominguezL (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: 243–251.

24. WatanabeA, TakedaK, PloplisB, TachibanaM (1998) Epistatic relationship between Waardenburg syndrome genes MITF and PAX3. Nat Genet 18: 283–286.

25. PotterfSB, FurumuraM, DunnKJ, ArnheiterH, PavanWJ (2000) Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum Genet 107: 1–6.

26. CurranK, RaibleDW, ListerJA (2009) Foxd3 controls melanophore specification in the zebrafish neural crest by regulation of Mitf. Dev Biol 332: 408–417.

27. IgnatiusMS, MooseHE, El-HodiriHM, HenionPD (2008) colgate/hdac1 Repression of foxd3 expression is required to permit mitfa-dependent melanogenesis. Dev Biol 313: 568–583.

28. ThomasAJ, EricksonCA (2009) FOXD3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Development 136: 1849–1858.

29. NitzanE, PfaltzgraffER, LaboskyPA, KalcheimC (2013) Neural crest and Schwann cell progenitor-derived melanocytes are two spatially segregated populations similarly regulated by Foxd3. Proc Natl Acad Sci U S A 110: 12709–12714.

30. TomitaH (1992) The lists of the mutants and strains of the medaka, common gambusia, silver crucian carp, goldfish, and golden venus fish maintained in the Laboratory of Freshwater Fish Stocks, Nagoya University. Fish Biol J MEDAKA 4: 45–47.

31. KelshRN, InoueC, MomoiA, KondohH, Furutani-SeikiM, et al. (2004) The Tomita collection of medaka pigmentation mutants as a resource for understanding neural crest cell development. Mech Dev 121: 841–859.

32. Tomita H (1975) In: Yamamoto T, editor. Medaka (KILLFISH): Biology and Strains. Tokyo: Keigaku Publishing Company. pp. 251–272.

33. Lynn LamoreuxM, KelshRN, WakamatsuY, OzatoK (2005) Pigment pattern formation in the medaka embryo. Pigment Cell Res 18: 64–73.

34. OdenthalJ, RossnagelK, HaffterP, KelshRN, VogelsangE, et al. (1996) Mutations affecting xanthophore pigmentation in the zebrafish, Danio rerio. Development 123: 391–398.

35. ParichyDM, RansomDG, PawB, ZonLI, JohnsonSL (2000) An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. Development 127: 3031–3044.

36. PelletierI, Bally-CuifL, ZieglerI (2001) Cloning and developmental expression of zebrafish GTP cyclohydrolase I. Mech Dev 109: 99–103.

37. KelshRN, SchmidB, EisenJS (2000) Genetic analysis of melanophore development in zebrafish embryos. Dev Biol 225: 277–293.

38. DuttonKA, PaulinyA, LopesSS, ElworthyS, CarneyTJ, et al. (2001) Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128: 4113–4125.

39. KelshRN, EisenJS (2000) The zebrafish colourless gene regulates development of non-ectomesenchymal neural crest derivatives. Development 127: 515–525.

40. CurranK, ListerJA, KunkelGR, PrendergastA, ParichyDM, et al. (2010) Interplay between Foxd3 and Mitf regulates cell fate plasticity in the zebrafish neural crest. Dev Biol 344: 107–118.

41. LopesSS, YangX, MullerJ, CarneyTJ, McAdowAR, et al. (2008) Leukocyte tyrosine kinase functions in pigment cell development. PLoS Genet 4: e1000026.

42. ObikaM (1996) Morphology of chromatophores of the medaka. Fish Biol J MEDAKA 8: 21–27.

43. LefebvreV (2010) The SoxD transcription factors–Sox5, Sox6, and Sox13–are key cell fate modulators. Int J Biochem Cell Biol 42: 429–432.

44. LefebvreV, LiP, de CrombruggheB (1998) A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J 17: 5718–5733.

45. StoltCC, LommesP, HillgartnerS, WegnerM (2008) The transcription factor Sox5 modulates Sox10 function during melanocyte development. Nucleic Acids Res 36: 5427–5440.

46. WatanabeK, TakedaK, YasumotoK, UdonoT, SaitoH, et al. (2002) Identification of a distal enhancer for the melanocyte-specific promoter of the MITF gene. Pigment Cell Res 15: 201–211.

47. LangD, LuMM, HuangL, EnglekaKA, ZhangM, et al. (2005) Pax3 functions at a nodal point in melanocyte stem cell differentiation. Nature 433: 884–887.

48. SchaferBW, CzernyT, BernasconiM, GeniniM, BusslingerM (1994) Molecular cloning and characterization of a human PAX-7 cDNA expressed in normal and neoplastic myocytes. Nucleic Acids Res 22: 4574–4582.

49. InabaM, YamanakaH, KondoS (2012) Pigment pattern formation by contact-dependent depolarization. Science 335: 677.

50. ParichyDM (2007) Homology and the evolution of novelty during Danio adult pigment pattern development. J Exp Zool B Mol Dev Evol 308: 578–590.

51. WadaH, ShimadaA, FukamachiS, NaruseK, ShimaA (1998) Sex-Linked Inheritance of the lf Locus in the Medaka Fish (Oryzias latipes). Zoolog Sci 15: 123–126.

52. HashimotoH, RebagliatiM, AhmadN, MuraokaO, KurokawaT, et al. (2004) The Cerberus/Dan-family protein Charon is a negative regulator of Nodal signaling during left-right patterning in zebrafish. Development 131: 1741–1753.

53. KimuraT, JindoT, NaritaT, NaruseK, KobayashiD, et al. (2004) Large-scale isolation of ESTs from medaka embryos and its application to medaka developmental genetics. Mech Dev 121: 915–932.

54. IshikawaT, KameiY, OtozaiS, KimJ, SatoA, et al. (2010) High-resolution melting curve analysis for rapid detection of mutations in a Medaka TILLING library. BMC Mol Biol 11: 70.

55. TaniguchiY, TakedaS, Furutani-SeikiM, KameiY, TodoT, et al. (2006) Generation of medaka gene knockout models by target-selected mutagenesis. Genome Biol 7: R116.