NF1 loss disrupts Schwann cell-axonal interactions: A novel role for semaphorin 4F

Genes and Development

Volumn 22, Issue 23, 2008, Pages 3335-3348

  Parrinello, Simona ^a   Noon, Luke A ^a   Harrisingh, Marie C ^b   Digby, Patrick Wingfield ^a   Rosenberg, Laura H ^a   Cremona, Catherine A ^a   Echave, Pedro ^a   Flanagan, Adrienne M ^c   Parada, Luis F ^d   Lloyd, Alison C ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ROYAL NATIONAL ORTHOPAEDIC HOSPITAL   (United Kingdom)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Heterotypic; NF1; Ras; Schwann cell axonal interactions; Semaphorins; Tumorigenesis

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NEUROFIBROMIN; RAF PROTEIN; RAS PROTEIN; SEMAPHORIN; SEMAPHORIN 4F; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL CONTACT; CELL INTERACTION; CELL PROLIFERATION; COCULTURE; DOWN REGULATION; HUMAN; MOLECULAR INTERACTION; NEOPLASM; NERVE FIBER; NEUROFIBROMA; NEUROFIBROMATOSIS; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SCHWANN CELL; UPREGULATION;

ANIMALS; AXONS; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; HUMANS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEUROFIBROMA; NEUROFIBROMIN 1; RATS; RATS, SPRAGUE-DAWLEY; SCHWANN CELLS; SEMAPHORINS;

EID: 57749101397     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.490608     Document Type: Article

References (42)

1. Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C.J., McLauchlan, H., Klevernic, I., Arthur, J.S., Alessi, D.R., and Cohen, P. 2007. The selectivity of protein kinase inhibitors: A further update. Biochem. J. 408: 297-315.
2. Basu, T.N., Gutmann, D.H., Fletcher, J.A., Glover, T.W., Collins, F.S., and Downward, J. 1992. Aberrant regulation of ras proteins in malignant tumour cells from type 1 neurofibromatosis patients. Nature 356: 713-715.
3. Casazza, A., Fazzari, P., and Tamagnone, L. 2007. Semaphorin signals in cell adhesion and cell migration: Functional role and molecular mechanisms. Adv. Exp. Med. Biol. 600: 90-108.
4. Chan, J.R., Jolicoeur, C., Yamauchi, J., Elliott, J., Fawcett, J.P., Ng, B.K., and Cayouette, M. 2006. The polarity protein Par-3 directly interacts with p75NTR to regulate myelination. Science 314: 832-836.
5. Cichowski, K. and Jacks, T. 2001. NF1 tumor suppressor gene function: Narrowing the GAP. Cell 104: 593-604.
6. Cohen, R.I., Rottkamp, D.M., Maric, D., Barker, J.L., and Hudson, L.D. 2003. A role for semaphorins and neuropilins in oligodendrocyte guidance. J. Neurochem. 85: 1262-1278.
7. Colman, S.D., Williams, C.A., and Wallace, M.R. 1995. Benign neurofibromas in type 1 neurofibromatosis (NF1) show somatic deletions of the NF1 gene. Nat. Genet. 11: 90-92.
8. Corfas, G., Velardez, M.O., Ko, C.P., Ratner, N., and Peles, E. 2004. Mechanisms and roles of axon-Schwann cell interactions. J. Neurosci. 24: 9250-9260.
9. Cowley, S., Paterson, H., Kemp, P., and Marshall, C.J. 1994. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77: 841-852.
10. DeClue, J.E., Papageorge, A.G., Fletcher, J.A., Diehl, S.R., Ratner, N., Vass, W.C., and Lowy, D.R. 1992. Abnormal regulation of mammalian p21ras contributes to malignant tumor growth in von Recklinghausen (type 1) neurofibromatosis. Cell 69: 265-273.
11. Encinas, J.A., Kikuchi, K., Chedotal, A., de Castro, F., Goodman, C.S., and Kimura, T. 1999. Cloning, expression, and genetic mapping of Sema W, a member of the semaphorin family. Proc. Natl. Acad. Sci. 96: 2491-2496.
12. Friedman, J.M. and Birch, P.H. 1997. Type 1 neurofibromatosis: A descriptive analysis of the disorder in 1,728 patients. Am. J. Med. Genet. 70: 138-143.
13. Harrisingh, M.C. and Lloyd, A.C. 2004. Ras/Raf/ERK signalling and NF1. Cell Cycle 3: 1255-1258.
14. Harrisingh, M.C., Perez-Nadales, E., Parkinson, D.B., Malcolm, D.S., Mudge, A.W., and Lloyd, A.C. 2004. The Ras/Raf/ERK signalling pathway drives Schwann cell dedifferentiation. EMBO J. 23: 3061-3071.
15. Hase, A., Saito, F., Yamada, H., Arai, K., Shimizu, T., and Matsumura, K. 2005. Characterization of glial cell line-derived neurotrophic factor family receptor α-1 in peripheral nerve Schwann cells. J. Neurochem. 95: 537-543.
16. Itoh, K., Fushiki, S., Kamiguchi, H., Arnold, B., Altevogt, P., and Lemmon, V. 2005. Disrupted Schwann cell-axon interactions in peripheral nerves of mice with altered L1-integrin interactions. Mol. Cell. Neurosci. 30: 131-136.
17. Jessen, K.R. and Mirsky, R. 2005. The origin and development of glial cells in peripheral nerves. Nat. Rev. Neurosci. 6: 671-682.
18. Joseph, N.M., Mosher, J.T., Buchstaller, J., Snider, P., McKeever, P.E., Lim, M., Conway, S.J., Parada, L.F., Zhu, Y., and Morrison, S.J. 2008. The loss of Nf1 transiently promotes self-renewal but not tumorigenesis by neural crest stem cells. Cancer Cell 13: 129-140.
19. Kim, H.A., Rosenbaum, T., Marchionni, M.A., Ratner, N., and DeClue, J.E. 1995. Schwann cells from neurofibromin deficient mice exhibit activation of p21ras, inhibition of cell proliferation and morphological changes. Oncogene 11: 325-335.
20. Kim, H.A., Ling, B., and Ratner, N. 1997. Nf1-deficient mouse Schwann cells are angiogenic and invasive and can be induced to hyperproliferate: Reversion of some phenotypes by an inhibitor of farnesyl protein transferase. Mol. Cell. Biol. 17: 862-872.
21. Kruger, R.P., Aurandt, J., and Guan, K.L. 2005. Semaphorins command cells to move. Nat. Rev. Mol. Cell Biol. 6: 789-800.
22. Lloyd, A.C., Obermuller, F., Staddon, S., Barth, C.F., McMahon, M., and Land, H. 1997. Cooperating oncogenes converge to regulate cyclin/cdk complexes. Genes & Dev. 11: 663-677.
23. Masuda, K., Furuyama, T., Takahara, M., Fujioka, S., Kurinami, H., and Inagaki, S. 2004. Sema4D stimulates axonal outgrowth of embryonic DRG sensory neurones. Genes Cells 9: 821-829.
24. Mathon, N.F., Malcolm, D.S., Harrisingh, M.C., Cheng, L., and Lloyd, A.C. 2001. Lack of replicative senescence in normal rodent glia. Science 291: 872-875.
25. Michailov, G.V., Sereda, M.W., Brinkmann, B.G., Fischer, T.M., Haug, B., Birchmeier, C., Role, L., Lai, C., Schwab, M.H., and Nave, K.A. 2004. Axonal neuregulin-1 regulates myelin sheath thickness. Science 304: 700-703.
26. Mitchell, P.J., Perez-Nadales, E., Malcolm, D.S., and Lloyd, A.C. 2003. Dissecting the contribution of p16(INK4A) and the Rb family to the Ras transformed phenotype. Mol. Cell. Biol. 23: 2530-2542.
27. Obremski, V.J., Johnson, M.I., and Bunge, M.B. 1993. Fibroblasts are required for Schwann cell basal lamina deposition and ensheathment of unmyelinated sympathetic neurites in culture. J. Neurocytol. 22: 102-117.
28. Riccardi, V.M. 1992. Neurofibromatosis: Phenotype, natural history and pathogenesis. The John Hopkins University Press, Baltimore, MD.
29. Rosenbaum, T., Kim, H.A., Boissy, Y.L., Ling, B., and Ratner, N. 1999. Neurofibromin, the neurofibromatosis type 1 Ras-GAP, is required for appropriate P0 expression and myelination. Ann. N. Y. Acad. Sci. 883: 203-214.
30. Rozen, S. and Skaletsky, H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132: 365-386.
31. Rubin, J.B. and Gutmann, D.H. 2005. Neurofibromatosis type 1 - a model for nervous system tumour formation? Nat. Rev. Cancer 5: 557-564.
32. Samuels, M.L., Weber, M.J., Bishop, J.M., and McMahon, M. 1993. 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. 13: 6241-6252.
33. Scherer, S. and Salzar, J. L. 2001. Axon-Schwann cell interactions during peripheral nerve degeneration and regeneration. Oxford University Press, Oxford, UK.
34. Serra, E., Rosenbaum, T., Winner, U., Aledo, R., Ars, E., Estivill, X., Lenard, H.G., and Lazaro, C. 2000. Schwann cells harbor the somatic NF1 mutation in neurofibromas: Evidence of two different Schwann cell subpopulations. Hum. Mol. Genet. 9: 3055-3064.
35. Taveggia, C., Zanazzi, G., Petrylak, A., Yano, H., Rosenbluth, J., Einheber, S., Xu, X., Esper, R.M., Loeb, J.A., Shrager, P., et al. 2005. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47: 681-694.
36. Wanner, I.B. and Wood, P.M. 2002. N-cadherin mediates axon-aligned process growth and cell-cell interaction in rat Schwann cells. J. Neurosci. 22: 4066-4079.
37. Wanner, I.B., Guerra, N.K., Mahoney, J., Kumar, A., Wood, P.M., Mirsky, R., and Jessen, K.R. 2006. Role of N-cadherin in Schwann cell precursors of growing nerves. Glia 54: 439-459.
38. Wong, J.T., Wong, S.T., and O'Connor, T.P. 1999. Ectopic semaphorin-1a functions as an attractive guidance cue for developing peripheral neurons. Nat. Neurosci. 2: 798-803.
39. Wood, P.M. and Bunge, R.P. 1975. Evidence that sensory axons are mitogenic for Schwann cells. Nature 256: 662-664.
40. Wu, J., Williams, J.P., Rizvi, T.A., Kordich, J.J., Witte, D., Meijer, D., Stemmer-Rachamimov, A.O., Cancelas, J.A., and Ratner, N. 2008. Plexiform and dermal neurofibromas and pigmentation are caused by Nf1 loss in desert hedgehogexpressing cells. Cancer Cell 13: 105-116.
41. Zheng, H., Chang, L., Patel, N., Yang, J., Lowe, L., Burns, D.K., and Zhu, Y. 2008. Induction of abnormal proliferation by nonmyelinating schwann cells triggers neurofibroma formation. Cancer Cell 13: 117-128.
42. Zhu, Y., Ghosh, P., Charnay, P., Burns, D.K., and Parada, L.F. 2002. Neurofibromas in NF1: Schwann cell origin and role of tumor environment. Science 296: 920-922.