A Critical Role for PDGFRα Signaling in Medial Nasal Process Development

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The primitive face is composed of neural crest cell (NCC) derived prominences. The medial nasal processes (MNP) give rise to the upper lip and vomeronasal organ, and are essential for normal craniofacial development, but the mechanism of MNP development remains largely unknown. PDGFRα signaling is known to be critical for NCC development and craniofacial morphogenesis. In this study, we show that PDGFRα is required for MNP development by maintaining the migration of progenitor neural crest cells (NCCs) and the proliferation of MNP cells. Further investigations reveal that PI3K/Akt and Rac1 signaling mediate PDGFRα function during MNP development. We thus establish PDGFRα as a novel regulator of MNP development and elucidate the roles of its downstream signaling pathways at cellular and molecular levels.

Vyšlo v časopise: A Critical Role for PDGFRα Signaling in Medial Nasal Process Development. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003851
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003851

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1. ChaiY, JiangX, ItoY, et al. (2000) Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127 : 1671–1679.

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

3. CorderoDR, BrugmannS, ChuY, BajpaiR, JameM, et al. (2011) Cranial neural crest cells on the move: their roles in craniofacial development. American Journal of Medical Genetics Part A 155A: 270–279.

4. GammillLS, Bronner-FraserM (2003) Neural crest specification: migrating into genomics. Nature Reviews Neuroscience 4 : 795–805.

5. WehbyGL, CassellCH (2010) The impact of orofacial clefts on quality of life and healthcare use and costs. Oral Diseases 16 : 3–10.

6. DixonMJ, MarazitaML, BeatyTH, MurrayJC (2011) Cleft lip and palate: understanding genetic and environmental influences. Nature Reviews Genetics 12 : 167–178.

7. HelmsJA, CorderoD, TapadiaMD (2005) New insights into craniofacial morphogenesis. Development 132 : 851–861.

8. JiangR, BushJO, LidralAC (2006) Development of the upper lip: morphogenetic and molecular mechanisms. Dev Dyn 235 : 1152–1166.

9. SantagatiF, RijliFM (2003) Cranial neural crest and the building of the vertebrate head. Nature Reviews Neuroscience 4 : 806–818.

10. Osumi-YamashitaN, NinomiyaY, EtoK, DoiH (1994) The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Developmental Biology 164 : 409–419.

11. SerbedzijaGN, Bronner-FraserM, FraserSE (1992) Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116 : 297–307.

12. JonesNC, TrainorPA (2005) Role of morphogens in neural crest cell determination. Journal of Neurobiology 64 : 388–404.

13. KulesaPM, BaileyCM, Kasemeier-KulesaJC, McLennanR (2010) Cranial neural crest migration: New rules for an old road. Developmental Biology 344 : 543–554.

14. MinouxM, RijliFM (2010) Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development 137 : 2605–2621.

15. NietoMA (2001) The early steps of neural crest development. Mechanisms of Development 105 : 27–35.

16. AndraeJ, GalliniR, BetsholtzC (2008) Role of platelet-derived growth factors in physiology and medicine. Genes and Development 22 : 1276–1312.

17. HochR, SorianoP (2003) Roles of PDGF in animal development. Development 130 : 4769–4784.

18. TallquistM, KazlauskasA (2004) PDGF signaling in cells and mice. Cytokine & Growth Factor Reviews 15 : 205–213.

19. SmithCL, TallquistMD (2010) PDGF function in diverse neural crest cell populations. Cell Adh Migr 4 : 561–566.

20. HeldinCH, WestermarkB (1999) Mechanism of Action and In Vivo Role of Platelet-Derived Growth Factor. Physiological reviews 79 : 1283–1316.

21. TallquistMD, SorianoP (2003) Cell autonomous requirement for PDGFR in populations of cranial and cardiac neural crest cells. Development 130 : 507.

22. SorianoP (1997) The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 124 : 2691–2700.

23. NewbernJ, ZhongJ, WickramasingheRS, LiX, WuY, et al. (2008) Mouse and human phenotypes indicate a critical conserved role for ERK2 signaling in neural crest development. Proceedings of the National Academy of Sciences of the United States of America 105 : 17115–17120.

24. KlinghofferRA, HamiltonTG, HochR, SorianoP (2002) An Allelic Series at the PDGFalphaR Locus Indicates Unequal Contributions of Distinct Signaling Pathways During Development. Developmental Cell 2 : 103–113.

25. EberhartJK, HeX, SwartzME, YanYL, SongH, et al. (2008) MicroRNA Mirn140 modulates Pdgf signaling during palatogenesis. Nature Genetics 40 : 290–298.

26. DanielianPS, MuccinoD, RowitchDH, MichaelSK, McMahonAP (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Current Biology 8 : 1323–S1322, 1323-1326, S1321-S1322.

27. NodenDM, TrainorPA (2005) Relations and interactions between cranial mesoderm and neural crest populations. Journal of Anatomy 207 : 575–601.

28. NodenDM, SchneiderRA (2006) Neural crest cells and the community of plan for craniofacial development: historical debates and current perspectives. Advances in Experimental Medicine and Biology 589 : 1–23.

29. HamiltonTG, KlinghofferRA, CorrinPD, SorianoP (2003) Evolutionary Divergence of Platelet-Derived Growth Factor Alpha Receptor Signaling Mechanisms. Molecular and Cellular Biology 23 : 4013–4025.

30. DingH, WuX, BostromH, KimI, WongN, et al. (2004) A specific requirement for PDGF-C in palate formation and PDGFR-alpha signaling. Nat Genet 36 : 1111–1116.

31. BeverdamA, BrouwerA, ReijnenM, KorvingJ, MeijlinkF (2001) Severe nasal clefting and abnormal embryonic apoptosis in Alx3/Alx4 double mutant mice. Development 128 : 3975.

32. CompagnucciC, FishJL, SchwarkM, TarabykinV, DepewMJ (2011) Pax6 regulates craniofacial form through its control of an essential cephalic ectodermal patterning center. Genesis 49 : 307–325.

33. SorianoP (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genetics 21 : 70.

34. KawakamiM, UmedaM, NakagataN, TakeoT, YamamuraK (2011) Novel migrating mouse neural crest cell assay system utilizing P0-Cre/EGFP fluorescent time-lapse imaging. BMC Developmental Biology 11 : 68.

35. RidleyAJ (2001) Rho GTPases and cell migration. Journal of Cell Science 114 : 2713–2722.

36. Etienne-MannevilleS, HallA (2002) Rho GTPases in cell biology. Nature 420 : 629–635.

37. KashishianA, KazlauskasA, CooperJA (1992) Phosphorylation sites in the PDGF receptor with different specificities for binding GAP and PI3 kinase in vivo. EMBO Journal 11 : 1373–1382.

38. RidleyAJ, HallA (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70 : 389–399.

39. HawkinsPT, EguinoaA, QiuRG, StokoeD, CookeFT, et al. (1995) PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase. Current Biology 5 : 393–403.

40. ZubiaurM, SanchoJ, TerhorstC, FallerDV (1995) A small GTP-binding protein, Rho, associates with the platelet-derived growth factor type-beta receptor upon ligand binding. Journal of Biological Chemistry 270 : 17221–17228.

41. FuchsS, HerzogD, SumaraG, Büchmann-MøllerS, CivenniG, et al. (2009) Stage-Specific Control of Neural Crest Stem Cell Proliferation by the Small Rho GTPases Cdc42 and Rac1. Cell Stem Cell 4 : 236–247.

42. ThomasPS, KimJ, NunezS, GlogauerM, KaartinenV (2010) Neural crest cell-specific deletion of Rac1 results in defective cell-matrix interactions and severe craniofacial and cardiovascular malformations. Developmental Biology 340 : 613–625.

43. GurniakCB, PerlasE, WitkeW (2005) The actin depolymerizing factor n-cofilin is essential for neural tube morphogenesis and neural crest cell migration. Developmental Biology 278 : 231–241.

44. HallA (2005) Rho GTPases and the control of cell behaviour. Biochemical Society Transactions 33 : 891–895.

45. PhillipsHM, PapoutsiT, SoenenH, Ybot-GonzalezP, HendersonDJ, et al. (2012) Neural crest cell survival is dependent on Rho kinase and is required for development of the mid face in mouse embryos. PLoS ONE 7: e37685.

46. FengH, HuB, LiuKW, LiY, LuX, et al. (2011) Activation of Rac1 by Src-dependent phosphorylation of Dock180(Y1811) mediates PDGFRalpha-stimulated glioma tumorigenesis in mice and humans. Journal of Clinical Investigation 121 : 4670–4684.

47. PickettEA, OlsenGS, TallquistMD (2008) Disruption of PDGFRalpha-initiated PI3K activation and migration of somite derivatives leads to spina bifida. Development 135 : 589–598.

48. FengH, LiuKW, GuoP, ZhangP, ChengT, et al. (2012) Dynamin 2 mediates PDGFRalpha-SHP-2-promoted glioblastoma growth and invasion. Oncogene 31 : 2691–2702.

49. St. AmandTR, ZhangY, SeminaEV, ZhaoX, HuYP, et al. (2000) Antagonistic signals between BMP4 and FGF8 define the expression of Pitx1 and Pitx2 in mouse tooth-forming anlage. Developmental biology 217 : 323–332.

50. BushJO, SorianoP (2010) Ephrin-B1 forward signaling regulates craniofacial morphogenesis by controlling cell proliferation across Eph-ephrin boundaries. Genes and Development 24 : 2068–2080.

51. Glaß M, Möller B, Zirkel A, Wächter K, Hüttelmaier S, et al.. (2011) Scratch Assay Analysis with Topology-Preserving Level Sets and Texture Measures. In: Vitrià J, Sanches J, Hernández M, editors. Pattern Recognition and Image Analysis: Springer Berlin Heidelberg. pp. 100–108.