A Central Role for the ERK-Signaling Pathway in Controlling Schwann Cell Plasticity and Peripheral Nerve Regeneration In Vivo

Neuron

Volumn 73, Issue 4, 2012, Pages 729-742

  Napoli, Ilaria ^a   Noon, Luke A ^a   Ribeiro, Sara ^a   Kerai, Ajay P ^a   Parrinello, Simona ^a   Rosenberg, Laura H ^a   Collins, Melissa J ^a   Harrisingh, Marie C ^a   White, Ian J ^a   Woodhoo, Ashwin ^b   Lloyd, Alison C ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MYELIN; RAF PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; BLOOD NERVE BARRIER; CELL DEDIFFERENTIATION; CELL TRANSPORT; CONTROLLED STUDY; DEMYELINATION; DISEASE SEVERITY; ENZYME ACTIVATION; IN VIVO STUDY; INFLAMMATION; INFLAMMATORY CELL; MALE; MOUSE; MYELINATION; NERVE CELL DEGENERATION; NERVE CELL PLASTICITY; NERVE REGENERATION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; SCHWANN CELL; SIGNAL TRANSDUCTION; TRANSGENE;

ANIMALS; ANIMALS, NEWBORN; BENZAMIDES; CELL MOVEMENT; CYCLIN D1; CYTOKINES; DIPHENYLAMINE; ESTROGEN ANTAGONISTS; GENE EXPRESSION REGULATION; LEUKOCYTES; MALE; MAP KINASE SIGNALING SYSTEM; MAST CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON; MOTOR ACTIVITY; MYELIN SHEATH; NERVE REGENERATION; NEUTROPHILS; PERIPHERAL NERVE INJURIES; PROTO-ONCOGENE PROTEINS C-RAF; REACTION TIME; RECEPTOR, NERVE GROWTH FACTOR; RECEPTORS, ESTROGEN; RECOVERY OF FUNCTION; SCHWANN CELLS; T-LYMPHOCYTES; TAMOXIFEN; TIME FACTORS;

EID: 84857316265     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.11.031     Document Type: Article

References (49)

1. Bradley J.L., Abernethy D.A., King R.H., Muddle J.R., Thomas P.K. Neural architecture in transected rabbit sciatic nerve after prolonged nonreinnervation. J. Anat. 1998, 192:529-538.
2. Chen Z.L., Yu W.M., Strickland S. Peripheral regeneration. Annu. Rev. Neurosci. 2007, 30:209-233.
3. Choi Y.K., Kim K.W. Blood-neural barrier: its diversity and coordinated cell-to-cell communication. BMB Reports 2008, 41:345-352.
4. Crawley J.N. Behavioral phenotyping strategies for mutant mice. Neuron 2008, 57:809-818.
5. Fischer S., Weishaupt A., Troppmair J., Martini R. Increase of MCP-1 (CCL2) in myelin mutant Schwann cells is mediated by MEK-ERK signaling pathway. Glia 2008, 56:836-843.
6. Groh J., Heinl K., Kohl B., Wessig C., Greeske J., Fischer S., Martini R. Attenuation of MCP-1/CCL2 expression ameliorates neuropathy in a mouse model for Charcot-Marie-Tooth 1X. Hum. Mol. Genet. 2010, 19:3530-3543.
7. Hall S. The response to injury in the peripheral nervous system. J. Bone Joint Surg. Br. 2005, 87:1309-1319.
8. Harrisingh M.C., Perez-Nadales E., Parkinson D.B., Malcolm D.S., Mudge A.W., Lloyd A.C. The Ras/Raf/ERK signalling pathway drives Schwann cell dedifferentiation. EMBO J. 2004, 23:3061-3071.
9. Huang Y., Sirkowski E.E., Stickney J.T., Scherer S.S. Prenylation-defective human connexin32 mutants are normally localized and function equivalently to wild-type connexin32 in myelinating Schwann cells. J. Neurosci. 2005, 25:7111-7120.
10. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
11. Jessen K.R., Mirsky R. Negative regulation of myelination: relevance for development, injury, and demyelinating disease. Glia 2008, 56:1552-1565.
12. Joseph N.M., Mosher J.T., Buchstaller J., Snider P., McKeever P.E., Lim M., Conway S.J., Parada L.F., Zhu Y., Morrison S.J. The loss of Nf1 transiently promotes self-renewal but not tumorigenesis by neural crest stem cells. Cancer Cell 2008, 13:129-140.
13. Kohl B., Fischer S., Groh J., Wessig C., Martini R. MCP-1/CCL2 modifies axon properties in a PMP22-overexpressing mouse model for Charcot-Marie-tooth 1A neuropathy. Am. J. Pathol. 2010, 176:1390-1399.
14. Lloyd A.C., Obermüller F., Staddon S., Barth C.F., McMahon M., Land H. Cooperating oncogenes converge to regulate cyclin/cdk complexes. Genes Dev. 1997, 11:663-677.
15. MacDonald J.M., Beach M.G., Porpiglia E., Sheehan A.E., Watts R.J., Freeman M.R. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 2006, 50:869-881.
16. Martini R., Fischer S., López-Vales R., David S. Interactions between Schwann cells and macrophages in injury and inherited demyelinating disease. Glia 2008, 56:1566-1577.
17. McClatchey A.I. Neurofibromatosis. Annu. Rev. Pathol. 2007, 2:191-216.
18. Medzhitov R. Inflammation 2010: new adventures of an old flame. Cell 2010, 140:771-776.
19. Meyer zu Hörste G., Hartung H.P., Kieseier B.C. From bench to bedside-experimental rationale for immune-specific therapies in the inflamed peripheral nerve. Nat. Clin. Pract. Neurol. 2007, 3:198-211.
20. Michailov G.V., Sereda M.W., Brinkmann B.G., Fischer T.M., Haug B., Birchmeier C., Role L., Lai C., Schwab M.H., Nave K.A. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004, 304:700-703.
21. Morris J.H., Hudson A.R., Weddell G. A study of degeneration and regeneration in the divided rat sciatic nerve based on electron microscopy. IV. Changes in fascicular microtopography, perineurium and endoneurial fibroblasts. Z. Zellforsch. Mikrosk. Anat. 1972, 124:165-203.
22. Mueller M., Leonhard C., Wacker K., Ringelstein E.B., Okabe M., Hickey W.F., Kiefer R. Macrophage response to peripheral nerve injury: the quantitative contribution of resident and hematogenous macrophages. Lab. Invest. 2003, 83:175-185.
23. Nadra K., de Preux Charles A.S., Médard J.J., Hendriks W.T., Han G.S., Grès S., Carman G.M., Saulnier-Blache J.S., Verheijen M.H., Chrast R. Phosphatidic acid mediates demyelination in Lpin1 mutant mice. Genes Dev. 2008, 22:1647-1661.
24. Nave K.A. Myelination and the trophic support of long axons. Nat. Rev. Neurosci. 2010, 11:275-283.
25. Newbern J.M., Li X., Shoemaker S.E., Zhou J., Zhong J., Wu Y., Bonder D., Hollenback S., Coppola G., Geschwind D.H., et al. Specific functions for ERK/MAPK signaling during PNS development. Neuron 2011, 69:91-105.
26. Parkinson D.B., Bhaskaran A., Arthur-Farraj P., Noon L.A., Woodhoo A., Lloyd A.C., Feltri M.L., Wrabetz L., Behrens A., Mirsky R., Jessen K.R. c-Jun is a negative regulator of myelination. J. Cell Biol. 2008, 181:625-637.
27. Parrinello S., Lloyd A.C. Neurofibroma development in NF1-insights into tumour initiation. Trends Cell Biol. 2009, 19:395-403.
28. Parrinello S., Noon L.A., Harrisingh M.C., Digby P.W., Rosenberg L.H., Cremona C.A., Echave P., Flanagan A.M., Parada L.F., Lloyd A.C. NF1 loss disrupts Schwann cell-axonal interactions: a novel role for semaphorin 4F. Genes Dev. 2008, 22:3335-3348.
29. Parrinello S., Napoli I., Ribeiro S., Digby P.W., Fedorova M., Parkinson D.B., Doddrell R.D., Nakayama M., Adams R.H., Lloyd A.C. EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell 2010, 143:145-155.
30. Perrin F.E., Lacroix S., Avilés-Trigueros M., David S. Involvement of monocyte chemoattractant protein-1, macrophage inflammatory protein-1alpha and interleukin-1beta in Wallerian degeneration. Brain 2005, 128:854-866.
31. Samuels M.L., Weber M.J., Bishop J.M., McMahon M. Conditional transformation of cells and rapid activation of the mitogen-activated protein kinase cascade by an estradiol-dependent human raf-1 protein kinase. Mol. Cell. Biol. 1993, 13:6241-6252.
32. Scherer S.S., Xu Y.T., Messing A., Willecke K., Fischbeck K.H., Jeng L.J. Transgenic expression of human connexin32 in myelinating Schwann cells prevents demyelination in connexin32-null mice. J. Neurosci. 2005, 25:1550-1559.
33. Sherman D.L., Brophy P.J. Mechanisms of axon ensheathment and myelin growth. Nat. Rev. Neurosci. 2005, 6:683-690.
34. Sheu J.Y., Kulhanek D.J., Eckenstein F.P. Differential patterns of ERK and STAT3 phosphorylation after sciatic nerve transection in the rat. Exp. Neurol. 2000, 166:392-402.
35. Solit D.B., Garraway L.A., Pratilas C.A., Sawai A., Getz G., Basso A., Ye Q., Lobo J.M., She Y., Osman I., et al. BRAF mutation predicts sensitivity to MEK inhibition. Nature 2006, 439:358-362.
36. Staser K., Yang F.C., Clapp D.W. Mast cells and the neurofibroma microenvironment. Blood 2010, 116:157-164.
37. Stoll G., Jander S., Myers R.R. Degeneration and regeneration of the peripheral nervous system: from Augustus Waller's observations to neuroinflammation. J. Peripher. Nerv. Syst. 2002, 7:13-27.
38. Suter U., Scherer S.S. Disease mechanisms in inherited neuropathies. Nat. Rev. Neurosci. 2003, 4:714-726.
39. Syed N., Reddy K., Yang D.P., Taveggia C., Salzer J.L., Maurel P., Kim H.A. Soluble neuregulin-1 has bifunctional, concentration-dependent effects on Schwann cell myelination. J. Neurosci. 2010, 30:6122-6131.
40. Tapinos N., Ohnishi M., Rambukkana A. ErbB2 receptor tyrosine kinase signaling mediates early demyelination induced by leprosy bacilli. Nat. Med. 2006, 12:961-966.
41. Taveggia C., Zanazzi G., Petrylak A., Yano H., Rosenbluth J., Einheber S., Xu X., Esper R.M., Loeb J.A., Shrager P., et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 2005, 47:681-694.
42. Toews A.D., Barrett C., Morell P. Monocyte chemoattractant protein 1 is responsible for macrophage recruitment following injury to sciatic nerve. J. Neurosci. Res. 1998, 53:260-267.
43. Tofaris G.K., Patterson P.H., Jessen K.R., Mirsky R. Denervated Schwann cells attract macrophages by secretion of leukemia inhibitory factor (LIF) and monocyte chemoattractant protein-1 in a process regulated by interleukin-6 and LIF. J. Neurosci. 2002, 22:6696-6703.
44. Vargas M.E., Watanabe J., Singh S.J., Robinson W.H., Barres B.A. Endogenous antibodies promote rapid myelin clearance and effective axon regeneration after nerve injury. Proc. Natl. Acad. Sci. USA 2010, 107:11993-11998.
45. Weerasuriya A. Patterns of change in endoneurial capillary permeability and vascular space during Wallerian degeneration. Brain Res. 1988, 445:181-187.
46. Woodhoo A., Alonso M.B., Droggiti A., Turmaine M., D'Antonio M., Parkinson D.B., Wilton D.K., Al-Shawi R., Simons P., Shen J., et al. Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat. Neurosci. 2009, 12:839-847.
47. Wu J., Williams J.P., Rizvi T.A., Kordich J.J., Witte D., Meijer D., Stemmer-Rachamimov A.O., Cancelas J.A., Ratner N. Plexiform and dermal neurofibromas and pigmentation are caused by Nf1 loss in desert hedgehog-expressing cells. Cancer Cell 2008, 13:105-116.
48. Zheng H., Chang L., Patel N., Yang J., Lowe L., Burns D.K., Zhu Y. Induction of abnormal proliferation by nonmyelinating schwann cells triggers neurofibroma formation. Cancer Cell 2008, 13:117-128.
49. Zochodne D.W. Neurobiology of Peripheral Nerve Regeneration 2008, Cambridge University Presss, New York. First Edition.