#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Distinct Requirements for Cranial Ectoderm and Mesenchyme-Derived Wnts in Specification and Differentiation of Osteoblast and Dermal Progenitors


The cranial bones and dermis differentiate from mesenchyme beneath the surface ectoderm. Fate selection in cranial mesenchyme requires the canonical Wnt effector molecule β-catenin, but the relative contribution of Wnt ligand sources in this process remains unknown. Here we show Wnt ligands are expressed in cranial surface ectoderm and underlying supraorbital mesenchyme during dermal and osteoblast fate selection. Using conditional genetics, we eliminate secretion of all Wnt ligands from cranial surface ectoderm or undifferentiated mesenchyme, to uncover distinct roles for ectoderm- and mesenchyme-derived Wnts. Ectoderm Wnt ligands induce osteoblast and dermal fibroblast progenitor specification while initiating expression of a subset of mesenchymal Wnts. Mesenchyme Wnt ligands are subsequently essential during differentiation of dermal and osteoblast progenitors. Finally, ectoderm-derived Wnt ligands provide an inductive cue to the cranial mesenchyme for the fate selection of dermal fibroblast and osteoblast lineages. Thus two sources of Wnt ligands perform distinct functions during osteoblast and dermal fibroblast formation.


Vyšlo v časopise: Distinct Requirements for Cranial Ectoderm and Mesenchyme-Derived Wnts in Specification and Differentiation of Osteoblast and Dermal Progenitors. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004152
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004152

Souhrn

The cranial bones and dermis differentiate from mesenchyme beneath the surface ectoderm. Fate selection in cranial mesenchyme requires the canonical Wnt effector molecule β-catenin, but the relative contribution of Wnt ligand sources in this process remains unknown. Here we show Wnt ligands are expressed in cranial surface ectoderm and underlying supraorbital mesenchyme during dermal and osteoblast fate selection. Using conditional genetics, we eliminate secretion of all Wnt ligands from cranial surface ectoderm or undifferentiated mesenchyme, to uncover distinct roles for ectoderm- and mesenchyme-derived Wnts. Ectoderm Wnt ligands induce osteoblast and dermal fibroblast progenitor specification while initiating expression of a subset of mesenchymal Wnts. Mesenchyme Wnt ligands are subsequently essential during differentiation of dermal and osteoblast progenitors. Finally, ectoderm-derived Wnt ligands provide an inductive cue to the cranial mesenchyme for the fate selection of dermal fibroblast and osteoblast lineages. Thus two sources of Wnt ligands perform distinct functions during osteoblast and dermal fibroblast formation.


Zdroje

1. JiangX (2002) Tissue Origins and Interactions in the Mammalian Skull Vault. Developmental Biology 241: 106–116.

2. HsuY-H, ZillikensMC, WilsonSG, FarberCR, DemissieS, et al. (2010) An integration of genome-wide association study and gene expression profiling to prioritize the discovery of novel susceptibility Loci for osteoporosis-related traits. PLoS Genet 6: e1000977.

3. TranTH, JarrellA, ZentnerGE, WelshA, BrownellI, et al. (2010) Role of canonical Wnt signaling/ß-catenin via Dermo1 in cranial dermal cell development. Development 137: 3973–3984.

4. YoshidaT, VivatbutsiriP, Morriss-KayG, SagaY, IsekiS (2008) Cell lineage in mammalian craniofacial mesenchyme. Mechanisms of Development 125: 797–808.

5. HardyMH (1992) The secret life of the hair follicle. Trends Genet 8: 55–61.

6. SchneiderRA, HelmsJA (2003) The cellular and molecular origins of beak morphology. Science 299: 565–568.

7. MerrillAE, EamesBF, WestonSJ, HeathT, SchneiderRA (2008) Mesenchyme-dependent BMP signaling directs the timing of mandibular osteogenesis. Development 135: 1223–1234.

8. HallBK (1981) The induction of neural crest-derived cartilage and bone by embryonic epithelia: an analysis of the mode of action of an epithelial-mesenchymal interaction. J Embryol Exp Morphol 64: 305–320.

9. ChenD, JarrellA, GuoC, LangR, AtitR (2012) Dermal -catenin activity in response to epidermal Wnt ligands is required for fibroblast proliferation and hair follicle initiation. Development 139: 1522–1533.

10. FuJ, HsuW (2012) Epidermal Wnt Controls Hair Follicle Induction by Orchestrating Dynamic Signaling Crosstalk between the Epidermis and Dermis. Journal of Investigative Dermatology 133: 890–898.

11. EamesBF, SchneiderRA (2005) Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development. Development 132: 1499–1509.

12. GoodnoughLH, ChangAT, TreloarC, YangJ, ScacheriPC, et al. (2012) Twist1 mediates repression of chondrogenesis by beta-catenin to promote cranial bone progenitor specification. Development 139: 4428–4438.

13. DayT, GuoX, GarrettbealL, YangY (2005) Wnt/β-Catenin Signaling in Mesenchymal Progenitors Controls Osteoblast and Chondrocyte Differentiation during Vertebrate Skeletogenesis. Dev Cell 8: 739–750.

14. HillT, SpaterD, TaketoM, BirchmeierW, HartmannC (2005) Canonical Wnt/β-Catenin Signaling Prevents Osteoblasts from Differentiating into Chondrocytes. Dev Cell 8: 727–738.

15. ZhongZ, Zylstra-DiegelCR, SchumacherCA, BakerJJ, CarpenterAC, et al. (2012) Wntless functions in mature osteoblasts to regulate bone mass. Proceedings of the National Academy of Sciences 109: E2197–E2204.

16. RichardsJB, RivadeneiraF, InouyeM, PastinenTM, SoranzoN, et al. (2008) Bone mineral density, osteoporosis, and osteoporotic fractures: a genome-wide association study. Lancet 371: 1505–1512.

17. WangX, Reid SuttonV, Omar Peraza-LlanesJ, YuZ, RosettaR, et al. (2007) Mutations in X-linked PORCN, a putative regulator of Wnt signaling, cause focal dermal hypoplasia. Nat Genet 39: 836–838.

18. RivadeneiraF, StyrkársdottirU, EstradaK, HalldórssonBV, HsuY-H, et al. (2009) Twenty bone-mineral-density loci identified by large-scale meta-analysis of genome-wide association studies. Nat Genet 41: 1199–1206.

19. BänzigerC, SoldiniD, SchüttC, ZipperlenP, HausmannG, et al. (2006) Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 125: 509–522.

20. BartschererK, PelteN, IngelfingerD, BoutrosM (2006) Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 125: 523–533.

21. FuJ, JiangM, MirandoAJ, YuHM, HsuW (2009) Reciprocal regulation of Wnt and Gpr177/mouse Wntless is required for embryonic axis formation. Proceedings of the National Academy of Sciences 106: 18598–18603.

22. GoodmanRM, ThombreS, FirtinaZ, GrayD, BettsD, et al. (2006) Sprinter: a novel transmembrane protein required for Wg secretion and signaling. Development 133: 4901–4911.

23. BelenkayaTY, WuY, TangX, ZhouB, ChengL, et al. (2008) The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell 14: 120–131.

24. Franch-MarroX, WendlerF, GuidatoS, GriffithJ, Baena-LopezA, et al. (2008) Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat Cell Biol 10: 170–177.

25. PortF, KusterM, HerrP, FurgerE, BänzigerC, et al. (2008) Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat Cell Biol 10: 178–185.

26. PortF, BaslerK (2010) Wnt trafficking: new insights into Wnt maturation, secretion and spreading. Traffic 11: 1265–1271.

27. YangP-T, LorenowiczMJ, SilhankovaM, CoudreuseDYM, BetistMC, et al. (2008) Wnt signaling requires retromer-dependent recycling of MIG-14/Wntless in Wnt-producing cells. Dev Cell 14: 140–147.

28. DasS, YuS, SakamoriR, StypulkowskiE, GaoN (2012) Wntless in Wnt secretion: molecular, cellular and genetic aspects. Front Biol (Beijing) 7: 587–593.

29. FuJ, Ivy YuH-M, MaruyamaT, MirandoAJ, HsuW (2011) Gpr177/mouse Wntless is essential for Wnt-mediated craniofacial and brain development. Dev Dyn 240: 365–371.

30. van AmerongenR, NusseR (2009) Towards an integrated view of Wnt signaling in development. Development 136: 3205–3214.

31. CleversH, NusseR (2012) Wnt/beta-catenin signaling and disease. Cell 149: 1192–1205.

32. SpaterD, HillTP, O'Sullivan RJ, GruberM, ConnerDA, et al. (2006) Wnt9a signaling is required for joint integrity and regulation of Ihh during chondrogenesis. Development 133: 3039–3049.

33. BennettCN, LongoKA, WrightWS, SuvaLJ, LaneTF, et al. (2005) Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci USA 102: 3324–3329.

34. AtitR, SgaierSK, MohamedOA, TaketoMM, DufortD, et al. (2006) Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Developmental Biology 296: 164–176.

35. OhtolaJ, MyersJ, Akhtar-ZaidiB, ZuzindlakD, SandesaraP, et al. (2008) beta-Catenin has sequential roles in the survival and specification of ventral dermis. Development 135: 2321–2329.

36. HuB, LefortK, QiuW, NguyenB-C, RajaramRD, et al. (2010) Control of hair follicle cell fate by underlying mesenchyme through a CSL-Wnt5a-FoxN1 regulatory axis. Genes & Development 24: 1519–1532.

37. LiL, CserjesiP, OlsonEN (1995) Dermo-1: a novel twist-related bHLH protein expressed in the developing dermis. Developmental Biology 172: 280–292.

38. CarpenterAC, RaoS, WellsJM, CampbellK, LangRA (2010) Generation of mice with a conditional null allele for Wntless. genesis 48: 554–558.

39. ReidBS, YangH, MelvinVS, TaketoMM, WilliamsT (2011) Ectodermal Wnt/beta-catenin signaling shapes the mouse face. Developmental Biology 349: 261–269.

40. YuK (2003) Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130: 3063–3074.

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

42. WillertK, BrownJD, DanenbergE, DuncanAW, WeissmanIL, et al. (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423: 448–452.

43. RudloffS, KemlerR (2012) Differential requirements for beta-catenin during mouse development. Development 139: 3711–3721.

44. LyonsJP, MuellerUW, JiH, EverettC, FangX, et al. (2004) Wnt-4 activates the canonical beta-catenin-mediated Wnt pathway and binds Frizzled-6 CRD: functional implications of Wnt/beta-catenin activity in kidney epithelial cells. Exp Cell Res 298: 369–387.

45. ZhengHF, TobiasJH, DuncanE, EvansDM, ErikssonJ, et al. (2012) WNT16 influences bone mineral density, cortical bone thickness, bone strength, and osteoporotic fracture risk. PLoS Genet 8: e1002745.

46. ManiP, JarrellA, MyersJ, AtitR (2010) Visualizing canonical Wnt signaling during mouse craniofacial development. Dev Dyn 239: 354–363.

47. FjeldK, KettunenPI, FurmanekT, KvinnslandIH, LuukkoK (2005) Dynamic expression of Wnt signaling-related Dickkopf1, -2, and -3 mRNAs in the developing mouse tooth. Dev Dyn 233: 161–166.

48. ZhuX, ZhuH, ZhangL, HuangS, CaoJ, et al. (2012) Wls-mediated Wnts differentially regulate distal limb patterning and tissue morphogenesis. Developmental Biology 1–11.

49. ZhouW, LinL, MajumdarA, LiX, ZhangX, et al. (2007) Modulation of morphogenesis by noncanonical Wnt signaling requires ATF/CREB family-mediated transcriptional activation of TGFbeta2. Nat Genet 39: 1225–1234.

50. MaruyamaT, JiangM, HsuW (2012) Gpr177, a novel locus for bone-mineral-density and osteoporosis, regulates osteogenesis and chondrogenesis in skeletal development. J Bone Miner Res 28: 1150–1159.

51. GrosJ, SerralboO, MarcelleC (2009) WNT11 acts as a directional cue to organize the elongation of early muscle fibres. Nature 457: 589–593.

52. GaoB, SongH, BishopK, ElliotG, GarrettL, et al. (2011) Wnt Signaling Gradients Establish Planar Cell Polarity by Inducing Vangl2 Phosphorylation through Ror2. Dev Cell 20: 163–176.

53. YamaguchiTP, BradleyA, McmahonAP, JonesS (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126: 1211–1223.

54. KibarZ, TorbanE, McDearmidJR, ReynoldsA, BerghoutJ, et al. (2007) Mutations in VANGL1 associated with neural-tube defects. N Engl J Med 356: 1432–1437.

55. LeiYP, ZhangT, LiH, WuBL, JinL, et al. (2010) VANGL2 mutations in human cranial neural-tube defects. N Engl J Med 362: 2232–2235.

56. GrzeschikK-H, BornholdtD, OeffnerF, KönigA, Del Carmen BoenteM, et al. (2007) Deficiency of PORCN, a regulator of Wnt signaling, is associated with focal dermal hypoplasia. Nat Genet 39: 833–835.

57. BarrottJJ, CashGM, SmithAP, BarrowJR, MurtaughLC (2011) Deletion of mouse Porcn blocks Wnt ligand secretion and reveals an ectodermal etiology of human focal dermal hypoplasia/Goltz syndrome. Proceedings of the National Academy of Sciences 108: 12752–12757.

58. PettiM, SamanichJ, PanQ, HuangCK, ReinmundJ, et al. (2011) Molecular characterization of an interstitial deletion of 1p31.3 in a patient with obesity and psychiatric illness and a review of the literature. Am J Med Genet A 155A: 825–832.

59. KimmelRA, TurnbullDH, BlanquetV, WurstW, LoomisCA, et al. (2000) Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes & Development 14: 1377–1389.

60. DassuleHR, LewisP, BeiM, MaasR, McmahonAP (2000) Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127: 4775–4785.

61. BraultV, MooreR, KutschS, IshibashiM, RowitchDH, et al. (2001) Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128: 1253–1264.

62. HaegelH, LarueL, OhsugiM, FedorovL, HerrenknechtK, et al. (1995) Lack of beta-catenin affects mouse development at gastrulation. Development 121: 3529–3537.

63. IshiiM, MerrillAE, ChanY-S, GitelmanI, RiceDPC, et al. (2003) Msx2 and Twist cooperatively control the development of the neural crest-derived skeletogenic mesenchyme of the murine skull vault. Development 130: 6131–6142.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 2
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#