Wnt/Rspondin/β-catenin signals control axonal sorting and lineage progression in Schwann cell development

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 45, 2013, Pages 18174-18179

  Grigoryan, Tamara ^a   Stein, Simone ^a   Qi, Jingjing ^a   Wende, Hagen ^a   Garratt, Alistair N ^b   Nave, Klaus Armin ^c   Birchmeier, Carmen ^a   Birchmeier, Walter ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

Axin2 LacZ reporter mice; Lamellipodia; Lgr5 receptor; Myelination; Paracrine mechanism

Indexed keywords

BETA CATENIN; PROTEIN; RSPONDIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; GENE EXPRESSION; LOSS OF FUNCTION MUTATION; MOLECULAR MECHANICS; MOUSE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL;

AXIN2-LACZ REPORTER MICE; LAMELLIPODIA; LGR5 RECEPTOR; MYELINATION; PARACRINE MECHANISM;

ANIMALS; AXONS; BETA CATENIN; BLOTTING, WESTERN; CELL LINEAGE; DNA PRIMERS; FLOW CYTOMETRY; IN SITU HYBRIDIZATION; MICE; MICE, TRANSGENIC; MICROARRAY ANALYSIS; MUTATION; PARACRINE COMMUNICATION; REAL-TIME POLYMERASE CHAIN REACTION; SCHWANN CELLS; SCIATIC NERVE; THROMBOSPONDINS; WNT SIGNALING PATHWAY;

EID: 84887305365     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1310490110     Document Type: Article

References (53)

1. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6(9):671-682.
2. Mirsky R, et al. (2008) Novel signals controlling embryonic Schwann cell development, myelination and dedifferentiation. J Peripher Nerv Syst 13(2):122-135.
3. Newbern J, Birchmeier C (2010) Nrg1/ErbB signaling networks in Schwann cell development and myelination. Semin Cell Dev Biol 21(9):922-928.
4. Grossmann KS, et al. (2009) The tyrosine phosphatase Shp2 (PTPN11) directs Neuregulin-1/ErbB signaling throughout Schwann cell development. Proc Natl Acad Sci USA 106(39):16704-16709.
5. Taveggia C, et al. (2005) Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47(5):681-694.
6. Birchmeier C, Nave KA (2008) Neuregulin-1, a key axonal signal that drives Schwann cell growth and differentiation. Glia 56(14):1491-1497.
7. Woodhoo A, et al. (2009) Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat Neurosci 12(7):839-847.
8. Feltri ML, et al. (2002) Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J Cell Biol 156(1):199-209.
9. Nodari A, et al. (2007) Beta1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination. J Cell Biol 177(6):1063-1075.
10. Finzsch M, et al. (2010) Sox10 is required for Schwann cell identity and progression beyond the immature Schwann cell stage. J Cell Biol 189(4):701-712.
11. Le N, et al. (2005) Analysis of congenital hypomyelinating Egr2Lo/Lo nerves identifies Sox2 as an inhibitor of Schwann cell differentiation and myelination. Proc Natl Acad Sci USA 102(7):2596-2601.
12. Clevers H, Nusse R (2012) Wnt/β-catenin signaling and disease. Cell 149(6):1192-1205.
13. Grigoryan T, Wend P, Klaus A, Birchmeier W (2008) Deciphering the function of canonical Wnt signals in development and disease: Conditional loss- and gain-of-function mutations of beta-catenin in mice. Genes Dev 22(17):2308-2341.
14. Brault V, 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(8):1253-1264.
15. Gammill LS, Bronner-Fraser M (2003) Neural crest specification: Migrating into genomics. Nat Rev Neurosci 4(10):795-805.
16. Hari L, et al. (2002) Lineage-specific requirements of beta-catenin in neural crest development. J Cell Biol 159(5):867-880.
17. Lee HY, et al. (2004) Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells. Science 303(5660):1020-1023.
18. Makoukji J, et al. (2011) Interplay between LXR and Wnt/β-catenin signaling in the negative regulation of peripheral myelin genes by oxysterols. J Neurosci 31(26):9620-9629.
19. Tawk M, et al. (2011) Wnt/beta-catenin signaling is an essential and direct driver of myelin gene expression and myelinogenesis. J Neurosci 31(10):3729-3742.
20. Gess B, et al. (2008) Inhibition of N-cadherin and beta-catenin function reduces axoninduced Schwann cell proliferation. J Neurosci Res 86(4):797-812.
21. Jacob C, et al. (2011) HDAC1 and HDAC2 control the transcriptional program of myelination and the survival of Schwann cells. Nat Neurosci 14(4):429-436.
22. Lewallen KA, et al. (2011) Assessing the role of the cadherin/catenin complex at the Schwann cell-axon interface and in the initiation of myelination. J Neurosci 31(8): 3032-3043.
23. Ye F, et al. (2009) HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12(7):829-838.
24. Carmon KS, Lin Q, Gong X, Thomas A, Liu Q (2012) LGR5 interacts and cointernalizes with Wnt receptors to modulate Wnt/β-catenin signaling.Mol Cell Biol 32(11):2054-2064.
25. de Lau WB, Snel B, Clevers HC (2012) The R-spondin protein family. Genome Biol 13(3):242.
26. Glinka A, et al. (2011) LGR4 and LGR5 are R-spondin receptors mediating Wnt/β-catenin and Wnt/PCP signalling. EMBO Rep 12(10):1055-1061.
27. Barker N, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449(7165):1003-1007.
28. Imada M, Sueoka N (1978) Clonal sublines of rat neurotumor RT4 and cell differentiation. I. Isolation and characterization of cell lines and cell type conversion. Dev Biol 66(1):97-108.
29. Molenaar M, et al. (1996) XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86(3):391-399.
30. Lustig B, et al. (2002) Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 22(4):1184-1193.
31. DasGupta R, Fuchs E (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126(20): 4557-4568.
32. Lappe-Siefke C, et al. (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33(3):366-374.
33. Huelsken J, Vogel R, Erdmann B, Cotsarelis G, Birchmeier W (2001) beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105(4):533-545.
34. Harada N, et al. (1999) Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 18(21):5931-5942.
35. Goebbels S, et al. (2010) Elevated phosphatidylinositol 3, 4, 5-trisphosphate in glia triggers cell-autonomous membrane wrapping and myelination. J Neurosci 30(26): 8953-8964.
36. Benninger Y, et al. (2007) Essential and distinct roles for cdc42 and rac1 in the regulation of Schwann cell biology during peripheral nervous system development. J Cell Biol 177(6):1051-1061.
37. Grove M, et al. (2007) FAK is required for axonal sorting by Schwann cells. J Cell Biol 176(3):277-282.
38. Peitz M, et al. (2007) Enhanced purification of cell-permeant Cre and germline transmission after transduction into mouse embryonic stem cells. Genesis 45(8):508-517.
39. Ring DB, et al. (2003) Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 52(3):588-595.
40. Eccleston PA, Mirsky R, Jessen KR, Sommer I, Schachner M (1987) Postnatal development of rat peripheral nerves: An immunohistochemical study of membrane lipids common to non-myelin forming Schwann cells, myelin forming Schwann cells and oligodendrocytes. Brain Res 432(2):249-256.
41. Rousset R, et al. (2001) Naked cuticle targets dishevelled to antagonize Wnt signal transduction. Genes Dev 15(6):658-671.
42. Feltri ML, Suter U, Relvas JB (2008) The function of RhoGTPases in axon ensheathment and myelination. Glia 56(14):1508-1517.
43. Woodhoo A, Sommer L (2008) Development of the Schwann cell lineage: From the neural crest to the myelinated nerve. Glia 56(14):1481-1490.
44. Relucio J, Tzvetanova ID, Ao W, Lindquist S, Colognato H (2009) Laminin alters fyn regulatory mechanisms and promotes oligodendrocyte development. J Neurosci 29(38):11794-11806.
45. Wang H, et al. (2012) Myosin II is a negative regulator of oligodendrocyte morphological differentiation. J Neurosci Res 90(8):1547-1556.
46. Parkinson DB, et al. (2008) c-Jun is a negative regulator of myelination. J Cell Biol 181(4):625-637.
47. Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109(1):61-73.
48. Hindley C, Philpott A (2012) Co-ordination of cell cycle and differentiation in the developing nervous system. Biochem J 444(3):375-382.
49. Wegner M (2000) Transcriptional control in myelinating glia: Flavors and spices. Glia 31(1):1-14.
50. Langseth AJ, et al. (2010) Wnts influence the timing and efficiency of oligodendrocyte precursor cell generation in the telencephalon. J Neurosci 30(40):13367-13372.
51. Srinivas S, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4.
52. Woodhoo A, Dean CH, Droggiti A, Mirsky R, Jessen KR (2004) The trunk neural crest and its early glial derivatives: A study of survival responses, developmental schedules and autocrine mechanisms. Mol Cell Neurosci 25(1):30-41.
53. Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44-57.