Tumor suppressor schwannomin/merlin is critical for the organization of schwann cell contacts in peripheral nerves

Journal of Neuroscience

Volumn 28, Issue 42, 2008, Pages 10472-10481

  Denisenko, Natalia ^a,b   Cifuentes Diaz, Carmen ^a,b   Irinopoulou, Theano ^a,b   Carnaud, Michèle ^a,b   Benoit, Evelyne ^c   Niwa Kawakita, Michiko ^d,e   Chareyre, Fabrice ^d,e   Giovannini, Marco ^d,e,f   Girault, Jean Antoine ^a,b   Goutebroze, Laurence ^a,b  

^a INSTITUT DU FER À MOULIN   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c LABORATOIRE DE NEUROBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

^d INSERM   (France)

^e UNIVERSITÉ PARIS DIDEROT   (France)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Internodes; Juxtaparanodes; Neurofibromatosis type 2; Nodes of ranvier; Paranodes; Schmidt lanterman incisures

Indexed keywords

MERLIN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CONTACT; CELL COUNT; CELL PROLIFERATION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYTOPLASM; GENE DELETION; MOUSE; MYELIN SHEATH; MYELINATION; NERVE FIBER; NEUROFIBROMATOSIS; NONHUMAN; NONMYELINATED NERVE; PERIPHERAL NERVE; PHRENIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RANVIER NODE; SCHWANN CELL; ANIMAL; BIOSYNTHESIS; CELL COMMUNICATION; COMPARATIVE STUDY; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALS; CELL COMMUNICATION; CELL PROLIFERATION; GENE DELETION; HUMANS; MICE; MICE, TRANSGENIC; NEUROFIBROMIN 2; PERIPHERAL NERVES; SCHWANN CELLS; TUMOR SUPPRESSOR PROTEINS;

EID: 54849407866     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2537-08.2008     Document Type: Article

References (54)

1. Arroyo EJ, Scherer SS (2000) On the molecular architecture of myelinated fibers. Histochem Cell Biol 113:1-18.
2. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W, St Martin M, Li J, Einheber S, Chesler M, Rosenbluth J, Salzer JL, Bellen HJ (2001) Axonglia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30:369-383.
3. Boyle ME, Berglund EO, Murai KK, Weber L, Peles E, Ranscht B (2001) Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 30:385-397.
4. Chang BJ, Cho IJ, Brophy PJ (2000) A study on the immunocytochemical localization of neurofascin in rat sciatic nerve. J Vet Sci 1:67-71.
5. Denisenko-Nehrbass N, Goutebroze L, Galvez T, Bonnon C, Stankoff B, Ezan P, Giovannini M, Faivre-Sarrailh C, Girault JA (2003) Association of Caspr/paranodin with tumour suppressor schwannomin/merlin and beta1 integrin in the central nervous system. J Neurochem 84:209-221.
6. Dupree JL, Girault JA, Popko B (1999) Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol 147:1145-1152.
7. Fannon AM, Sherman DL, Ilyina-Gragerova G, Brophy PJ, Friedrich VL Jr, Colman DR (1995) Novel E-cadherin-mediated adhesion in peripheral nerve: Schwann cell architecture is stabilized by autotypic adherens junctions. J Cell Biol 129:189-202.
8. Fernandez-Valle C, Tang Y, Ricard J, Rodenas-Ruano A, Taylor A, Hackler E, Biggerstaff J, Iacovelli J (2002) Paxillin binds schwannomin and regulates its density-dependent localization and effect on cell morphology. Nat Genet 31:354-362.
9. Friede RL (1983) Variance in relative internode length (l/d) in the rat and its presumed significance for the safety factor and neuropathy. J Neurol Sci 60:89-104.
10. Garratt AN, Voiculescu O, Topilko P, Charnay P, Birchmeier C (2000) A dual role of erbB2 in myelination and in expansion of the schwann cell precursor pool. J Cell Biol 148:1035-1046.
11. Gatzinsky KP, Berthold CH, Rydmark M (1991) Axon-Schwann cell networks are regular components of nodal regions in normal large nerve fibres of cat spinal roots. Neurosci Lett 124:264-268.
12. Giovannini M, Robanus-Maandag E, Niwa-Kawakita M, van der Valk M, Woodruff JM, Goutebroze L, Mérel P, Berns A, Thomas G (1999) Schwann cell hyperplasia and tumors in transgenic mice expressing a naturally occurring mutant NF2 protein. Genes Dev 13:978-986.
13. Giovannini M, Robanus-Maandag E, van der Valk M, Niwa-Kawakita M, Abramowski V, Goutebroze L, Woodruff JM, Berns A, Thomas G (2000) Conditional biallelic Nf2 mutation in the mouse promotes manifestations of human neurofibromatosis type 2. Genes Dev 14:1617-1630.
14. Girault JA, Peles E (2002) Development of nodes of Ranvier. Curr Opin Neurobiol 12:476-485.
15. Gould RM, Byrd AL, Barbarese E (1995) The number of Schmidt-Lanterman incisures is more than doubled in shiverer PNS myelin sheaths. J Neurocytol 24:85-98.
16. Goutebroze L, Carnaud M, Denisenko N, Boutterin MC, Girault JA (2003) Syndecan-3 and syndecan-4 are enriched in Schwann cell perinodal processes. BMC Neurosci 4:29.
17. Grove M, Komiyama NH, Nave KA, Grant SG, Sherman DL, Brophy PJ (2007) FAK is required for axonal sorting by Schwann cells. J Cell Biol 176:277-282.
18. Hoshi T, Suzuki A, Hayashi S, Tohyama K, Hayashi A, Yamaguchi Y, Takeuchi K, Baba H (2007) Nodal protrusions, increased Schmidt-Lanterman incisures, and paranodal disorganization are characteristic features of sulfatide-deficient peripheral nerves. Glia 55:584-594.
19. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6:671-682.
20. Kalamarides M, Niwa-Kawakita M, Leblois H, Abramowski V, Perricaudet M, Janin A, Thomas G, Gutmann DH, Giovannini M (2002) Nf2 gene inactivation in arachnoidal cells is rate-limiting for meningioma development in the mouse. Genes Dev 16:1060-1065.
21. Kordeli E, Davis J, Trapp B, Bennett V (1990) An isoform of ankyrin is localized at nodes of Ranvier in myelinated axons of central and peripheral nerves. J Cell Biol 110:1341-1352.
22. Lallemand D, Curto M, Saotome I, Giovannini M, McClatchey AI (2003) NF2 deficiency promotes tumorigenesis and metastasis by destabilizing adherens junctions. Genes Dev 17:1090-1100.
23. Mathis C, Denisenko-Nehrbass N, Girault JA, Borrelli E (2001) Essential role of oligodendrocytes in the formation and maintenance of central nervous system nodal regions. Development 128:4881-4890.
24. McClatchey AI, Giovannini M (2005) Membrane organization and tumorigenesis - the NF2 tumor suppressor, merlin. Genes Dev 19:2265-2277.
25. McClatchey AI, Saotome I, Mercer K, Crowley D, Gusella JF, Bronson RT, Jacks T (1998) Mice heterozygous for a mutation at the Nf2 tumor suppressor locus develop a range of highly metastatic tumors. Genes Dev 12:1121-1133.
26. Melendez-Vasquez CV, Rios JC, Zanazzi G, Lambert S, Bretscher A, Salzer JL (2001) Nodes of Ranvier form in association with ezrin-radixin-moesin (ERM)-positive Schwann cell processes. Proc Natl Acad Sci U S A 98:1235-1240.
27. Menegoz M, Gaspar P, Le Bert M, Galvez T, Burgaya F, Palfrey C, Ezan P, Arnos F, Girault JA (1997) Paranodin, a glycoprotein of neuronal paranodal membranes. Neuron 19:319-331.
28. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave KA (2004) Axonal neuregulin-1 regulates myelin sheath thickness. Science 304:700-703.
29. Morrison H, Sperka T, Manent J, Giovannini M, Ponta H, Herrlich P (2007) Merlin/neurofibromatosis type 2 suppresses growth by inhibiting the activation of Ras and Rac. Cancer Res 67:520-527.
30. Neuberg DH, Sancho S, Suter U (1999) Altered molecular architecture of peripheral nerves in mice lacking the peripheral myelin protein 22 or connexin32. J Neurosci Res 58:612-623.
31. Obremski VJ, Hall AM, Fernandez-Valle C (1998) Merlin, the neurofibromatosis type 2 gene product, and beta1 integrin associate in isolated and differentiating Schwann cells. J Neurobiol 37:487-501.
32. Okada T, Lopez-Lago M, Giancotti FG (2005) Merlin/NF-2 mediates contact inhibition of growth by suppressing recruitment of Rac to the plasma membrane. J Cell Biol 171:361-371.
33. Okada T, You L, Giancotti FG (2007) Shedding light on Merlin's wizardry. Trends Cell Biol 17:222-229.
34. Perrin-Tricaud C, Rutishauser U, Tricaud N (2007) P120 catenin is required for thickening of Schwann cell myelin. Mol Cell Neurosci 35:120-129.
35. Poliak S, Peles E (2003) The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci 4:968-980.
36. Poliak S, Gollan L, Salomon D, Berglund EO, Ohara R, Ranscht B, Peles E (2001) Localization of Caspr2 in myelinated nerves depends on axon-glia interactions and the generation of barriers along the axon. J Neurosci 21:7568-7575.
37. Poulikakos PI, Xiao GH, Gallagher R, Jablonski S, Jhanwar SC, Testa JR (2006) Re-expression of the tumor suppressor NF2/merlin inhibits invasiveness in mesothelioma cells and negatively regulates FAK. Oncogene 25:5960-5968.
38. Rangwala R, Banine F, Borg JP, Sherman LS (2005) Erbin regulates mitogen-activated protein (MAP) kinase activation and MAP kinase-dependent interactions between Merlin and adherens junction protein complexes in Schwann cells. J Biol Chem 280:11790-11797.
39. Robertson JD (1958) The ultrastructure of Schmidt-Lanterman clefts and related shearing defects of the myelin sheath. J Biophys Biochem Cytol 4:39-46.
40. Rouleau GA, Merel P, Lutchman M, Sanson M, Zucman J, Marineau C, Hoang-Xuan K, Demczuk S, Desmaze C, Plougastel B, Pulst SM, Lenoir G, Bijlsma E, Fashold R, Dumanski J, de Jong P, Parry D, Eldridge R, Aurias A, Delattre O, Thomas G (1993) Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature 363:515-521.
41. Salzer JL (2003) Polarized domains of myelinated axons. Neuron 40:297-318.
42. Schafer DP, Bansal R, Hedstrom KL, Pfeiffer SE, Rasband MN (2004) Does paranode formation and maintenance require partitioning of neurofascin 155 into lipid rafts? J Neurosci 24:3176-3185.
43. Scherer SS, Gutmann DH (1996) Expression of the neurofibromatosis 2 tumor suppressor gene product, merlin, in Schwann cells. J Neurosci Res 46:595-605.
44. Sharghi-Namini S, Turmaine M, Meier C, Sahni V, Umehara F, Jessen KR, Mirsky R (2006) The structural and functional integrity of peripheral nerves depends on the glial-derived signal desert hedgehog. J Neurosci 26:6364-6376.
45. Shaw RJ, Paez JG, Curto M, Yaktine A, Pruitt WM, Saotome I, O'Bryan JP, Gupta V, Ratner N, Der CJ, Jacks T, McClatchey AI (2001) The Nf2 tumor suppressor, merlin, functions in Rac-dependent signaling. Dev Cell 1:63-72.
46. Sherman DL, Brophy PJ (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6:683-690.
47. Sperfeld AD, Hein C, Schröder JM, Ludolph AC, Hanemann CO (2002) Occurrence and characterization of peripheral nerve involvement in neurofibromatosis type 2. Brain 125:996-1004.
48. Stickney JT, Bacon WC, Rojas M, Ratner N, Ip W (2004) Activation of the tumor suppressor merlin modulates its interaction with lipid rafts. Cancer Res 64:2717-2724.
49. Tait S, Gunn-Moore F, Collinson JM, Huang J, Lubetzki C, Pedraza L, Sherman DL, Colman DR, Brophy PJ (2000) An oligodendrocyte cell adhesion molecule at the site of assembly of the paranodal axo-glial junction. J Cell Biol 150:657-666.
50. Taylor AR, Geden SE, Fernandez-Valle C (2003) Formation of a beta1 integrin signaling complex in Schwann cells is independent of rho. Glia 41:94-104.
51. Tricaud N, Perrin-Tricaud C, Brusés JL, Rutishauser U (2005) Adherens junctions in myelinating Schwann cells stabilize Schmidt-Lanterman incisures via recruitment of p120 catenin to E-cadherin. J Neurosci 25:3259-3269.
52. Trofatter JA, MacCollin MM, Rutter JL, Murrell JR, Duyao MP, Parry DM, Eldridge R, Kley N, Menon AG, Pulaski K, Haase VH, Ambrose CM, Munroe D, Bove C, Haines JL, Martuza RL, MacDonald ME, Seizenger BR, Short MP, Buckler AJ, Gusella JF (1993) A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 72:791-800.
53. + channels in terminal and juxtaparanodal regions of neurons. Nature 365:75-79.
54. Zhang SM, Marsh R, Ratner N, Brackenbury R (1995) Myelin glycoprotein P0 is expressed at early stages of chicken and rat embryogenesis. J Neurosci Res 40:241-250.