Neuropathy-associated Egr2 mutants disrupt cooperative activation of myelin protein zero by Egr2 and Sox10

Molecular and Cellular Biology

Volumn 27, Issue 9, 2007, Pages 3521-3529

  LeBlanc, Scott E ^a   Ward, Rebecca M ^b   Svaren, John ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 2; MUTANT PROTEIN; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN PROTEIN; TRANSCRIPTION FACTOR SOX10;

ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; GENE MUTATION; INTRON; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; RAT; SCIATIC NERVE;

ANIMALS; BINDING SITES; DNA-BINDING PROTEINS; DOWN-REGULATION; EARLY GROWTH RESPONSE PROTEIN 2; HIGH MOBILITY GROUP PROTEINS; INTRONS; MICE; MUTATION; MYELIN P0 PROTEIN; PERIPHERAL NERVOUS SYSTEM DISEASES; PROTEIN BINDING; RATS; SENSITIVITY AND SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 34247554140     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01689-06     Document Type: Article

References (53)

1. Aquino, J. B., J. Hjerling-Leffler, M. Koltzenburg, T. Edlund, M. J. Villar, and P. Ernfors. 2006. In vitro and in vivo differentiation of boundary cap neural crest stem cells into mature Schwann cells. Exp. Neurol. 198:438-449.
2. Arthur-Farraj, P., R. Mirsky, D. B. Parkinson, and K. R. Jessen. 2006. A double point mutation in the DNA-binding region of Egr2 switches its function from inhibition to induction of proliferation: a potential contribution to the development of congenital hypomyelinating neuropathy. Neurobiol. Dis. 24:159-169.
3. Bellone, E., E. Di Maria, S. Soriani, A. Varese, L. L. Doria, F. Ajmar, and P. Mandich. 1999. A novel mutation (D305V) in the early growth response 2 gene is associated with severe Charcot-Marie-Tooth type 1 disease. Hum. Mutat. 14:353-354.
4. Bondurand, N., M. Girard, V. Pingault, N. Lemort, O. Dubourg, and M. Goossens. 2001. Human Connexin 32, a gap junction protein altered in the X-linked form of Charcot-Marie-Tooth disease, is directly regulated by the transcription factor SOX10. Hum. Mol. Genet. 10:2783-2795.
5. Britsch, S., D. E. Goerich, D. Riethmacher, R. I. Peirano, M. Rossner, K. A. Nave, C. Birchmeier, and M. Wegner. 2001. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 15:66-78.
6. Brown, A. M., and G. Lemke. 1997. Multiple regulatory elements control transcription of the peripheral myelin protein zero gene. J. Biol. Chem. 272:28939-28947.
7. Feltri, M. L., M. D'Antonio, A. Quattrini, R. Numerato, M. Arona, S. Previtali, S. Y. Chiu, A. Messing, and L. Wrabetz. 1999. A novel P0 glycoprotein transgene activates expression of lacZ in myelin-forming Schwann cells. Eur. J. Neurosci. 11:1577-1586.
8. Ghislain, J., and P. Charnay. 2006. Control of myelination in Schwann cells: a Krox20 cis-regulatory element integrates Oct6, Brn2 and Sox10 activities. EMBO Rep. 7:52-58.
9. Ghislain, J., C. Desmarquet-Trin-Dinh, P. Gilardi-Hebenstreit, P. Charnay, and M. Frain. 2003. Neural crest patterning: autoregulatory and crest-specific elements co-operate for Krox20 transcriptional control. Development 130:941-953.
10. Ghislain, J., C. Desmarquet-Trin-Dinh, M. Jaegle, D. Meijer, P. Charnay, and M. Frain. 2002. Characterisation of cis-acting sequences reveals a biphasic, axon-dependent regulation of Krox20 during Schwann cell development. Development 129:155-166.
11. Gillian, A. L., and J. Svaren. 2004. The Ddx20/DP103 dead box protein represses transcriptional activation by Egr2/Krox-20. J. Biol. Chem. 279:9056-9063.
12. Hai, M., N. Muja, G. H. DeVries, R. H. Quarles, and P. I. Patel. 2002. Comparative analysis of Schwann cell lines as model systems for myelin gene transcription studies. J. Neurosci. Res. 69:497-508.
13. He, T. C., S. Zhou, L. T. da Costa, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509-2514.
14. Houlden, H., M. Girard, C. Cockerell, D. Ingram, N. W. Wood, M. Goossens, R. W. Walker, and M. M. Reilly. 2004. Connexin 32 promoter P2 mutations: a mechanism of peripheral nerve dysfunction. Ann. Neurol. 56:730-734.
15. Inoue, K., M. Khajavi, T. Ohyama, S. Hirabayashi, J. Wilson, J. D. Reggin, P. Maneias, I. J. Butler, M. F. Wilkinson, M. Wegner, and J. R. Lupski. 2004. Molecular mechanism for distinct neurological phenotypes conveyed by allelic truncating mutations. Nat. Genet. 36:361-369.
16. Jang, S. W., S. E. LeBlanc, A. Roopra, L. Wrabetz, and J. Svaren. 2006. In vivo detection of Egr2 binding to target genes during peripheral nerve myelination. J. Neurochem. 98:1678-1687.
17. Kamachi, Y., M. Uchikawa, and H. Kondoh. 2000. Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet. 16:182-187.
18. Kamaraju, A. K., C. Bertolotto, J. Chebath, and M. Revel. 2002. Pax3 down-regulation and shut-off of melanogenesis in melanoma B16/F10.9 by interleukin-6 receptor signaling. J. Biol. Chem. 277:15132-15141.
19. Kuhlbrodt, K., B. Herbarth, E. Sock, J. Enderich, I. Hermans-Borgmeyer, and M. Wegner. 1998. Cooperative function of POU proteins and SOX proteins in glial cells. J. Biol. Chem. 273:16050-16057.
20. Kuhlbrodt, K., B. Herbarth, E. Sock, I. Hermans-Borgmeyer, and M. Wegner. 1998. Sox10, a novel transcriptional modulator in glial cells. J. Neurosci. 18:237-250.
21. Kuhlbrodt, K., C. Schmidt, E. Sock, V. Pingault, N. Bondurand, M. Goossens, and M. Wegner. 1998. Functional analysis of Sox10 mutations found in human Waardenburg-Hirschsprung patients. J. Biol. Chem. 273:23033- 23038.
22. Le, N., R. Nagarajan, J. Y. Wang, T. Araki, R. E. Schmidt, and J. Milbrandt. 2005. Analysis of congenital hypomyelinating Egr2Lo/Lo nerves identifies Sox2 as an inhibitor of Schwann cell differentiation and myelination. Proc. Natl. Acad. Sci. USA 102:2596-2601.
23. Le, N., R. Nagarajan, J. Y. Wang, J. Svaren, C. LaPash, T. Araki, R. E. Schmidt, and J. Milbrandt. 2005. Nab proteins are essential for peripheral nervous system myelination. Nat. Neurosci. 8:932-940.
24. LeBlanc, S. E., S. W. Jang, R. M. Ward, L. Wrabetz, and J. Svaren. 2006. Direct regulation of myelin protein zero expression by the Egr2 transactivator. 1. Biol. Chem. 281:5453-5460.
25. LeBlanc, S. E., R. Srinivasan, C. Ferri, G. M. Mager, A. L. Gillian-Daniel, L. Wrabetz, and J. Svaren. 2005. Regulation of cholesterol/lipid biosynthetic genes by Egr2/Krox20 during peripheral nerve myelination. J. Neurochem. 93:737-748.
26. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
27. Loots, G. G., I. Ovcharenko, L. Pachter, I. Dubchak, and E. M. Rubin. 2002. rVista for comparative sequence-based discovery of functional transcription factor binding sites. Genome Res. 12:832-839.
28. Martini, R., J. Zielasek, K. V. Toyka, K. P. Giese, and M. Schachner. 1995. Protein zero (P0)-deficient mice show myelin degeneration in peripheral nerves characteristic of inherited human neuropathies. Nat. Genet. 11:281-286.
29. Mikesova, E., K. Huhne, B. Rautenstrauss, R. Mazanec, L. Barankova, M. Vyhnalek, O. Horacek, and P. Seeman. 2005. Novel EGR2 mutation R359Q is associated with CMT type 1 and progressive scoliosis. Neuromuscul. Disord. 15:764-767.
30. Musso, M., P. Balestra, E. Bellone, D. Cassandrini, E. Di Maria, L. L. Doria, M. Grandis, G. L. Mancardi, A. Schenone, G. Levi, F. Ajmar, and P. Mandich. 2001. The D355V mutation decreases EGR2 binding to an element within the Cx32 promoter. Neurobiol. Dis. 8:700-706.
31. Musso, M., P. Balestra, F. Taroni, E. Bellone, and P. Mandich. 2003. Different consequences of EGR2 mutants on the transactivation of human Cx32 promoter. Neurobiol. Dis. 12:89-95.
32. Nagarajan, R., J. Svaren, N. Le, T. Araki, M. Watson, and J. Milbrandt. 2001. EGR2 mutations in inherited neuropathies dominant-negatively inhibit myelin gene expression. Neuron 30:355-368.
33. Paratore, C., D. E. Goerich, U. Suter, M. Wegner, and L. Sommer. 2001. Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128:3949-3961.
34. Pareyson, D., F. Taroni, S. Botti, M. Morbin, S. Baratta, G. Lauria, C. Ciano, and A. Sghirlanzoni. 2000. Cranial nerve involvement in CMT disease type 1 due to early growth response 2 gene mutation. Neurology 54:1696-1698.
35. Parkinson, D. B., A. Bhaskaran, A. Droggiti, S. Dickinson, M. D'Antonio, R. Mirsky, and K. R. Jessen. 2004. Krox-20 inhibits Jun-NH2-terminal kinase/c-Jun to control Schwann cell proliferation and death. J. Cell Biol. 164:385-394.
36. Parkinson, D. B., S. Dickinson, A. Bhaskaran, M. T. Kinsella, P. J. Brophy, D. L. Sherman, S. Sharghi-Namini, M. B. Duran Alonso, R. Mirsky, and K. R. Jessen. 2003. Regulation of the myelin gene periaxin provides evidence for Krox-20-independent myelin-related signalling in Schwann cells. Mol. Cell. Neurosci. 23:13-27.
37. Peirano, R. I., D. E. Goerich, D. Riethmacher, and M. Wegner. 2000. Protein zero gene expression is regulated by the glial transcription factor Sox10. Mol. Cell. Biol. 20:3198-3209.
38. Peirano, R. I., and M. Wegner. 2000. The glial transcription factor Sox10 binds to DNA both as monomer and dimer with different functional consequences. Nucleic Acids Res. 28:3047-3055.
39. Sevetson, B. R., J. Svaren, and J. Milbrandt. 2000. A novel activation function for NAB proteins in EGR-dependent transcription of the luteinizing hormone beta gene. J. Biol. Chem. 275:9749-9757.
40. Shy, M. E. 2005. HMSN related to MPZ (P0) mutations, p. 1681-1706. In P. J. Dyck and P. K. Thomas (ed.), Peripheral neuropathy. W. B. Saunders, Philadelphia, PA.
41. Slutsky, S. G., A. K. Kamaraju, A. M. Levy, J. Chebath, and M. Revel. 2003. Activation of myelin genes during transdifferentiation from melanoma to glial cell phenotype. J. Biol. Chem. 278:8960-8968.
42. Stahl, N., J. Harry, and B. Popko. 1990. Quantitative analysis of myelin protein gene expression during development in the rat sciatic nerve. Brain Res. Mol. Brain Res. 8:209-212.
43. Timmerman, V., P. De Jonghe, C. Ceuterick, E. De Vriendt, A. Lofgren, E. Nelis, L. E. Warner, J. R. Lupski, J. J. Martin, and C. Van Broeckhoven. 1999. Novel missense mutation in the early growth response 2 gene associated with Dejerine-Sottas syndrome phenotype. Neurology 52:1827-1832.
44. Toda, K., J. A. Small, S. Goda, and R. H. Quarles. 1994. Biochemical and cellular properties of three immortalized Schwann cell lines expressing different levels of the myelin-associated glycoprotein. J. Neurochem. 63:1646-1657.
45. Topilko, P., S. Schneider-Maunoury, G. Levi, A. Baron-Van Evercooren, A. B. Chennoufi, T. Seitanidou, C. Babinet, and P. Charnay. 1994. Krox-20 controls myelination in the peripheral nervous system. Nature 371:796-799.
46. Warner, L. E., P. Mancias, I. J. Butler, C. M. McDonald, L. Keppen, K. G. Koob, and J. R. Lupski. 1998. Mutations in the early growth response 2 (EGR2) gene are associated with hereditary myelinopathies. Nat. Genet. 18:382-384.
47. Warner, L. E., J. Svaren, J. Milbrandt, and J. R. Lupski. 1999. Functional consequences of mutations in the early growth response 2 gene (EGR2) correlate with severity of human myelinopathies. Hum. Mol. Genet. 8:1245-1251.
48. Wegner, M. 2005. Secrets to a healthy Sox life: lessons for melanocytes. Pigment Cell Res. 18:74-85.
49. Wilson, M., and P. Koopman. 2002. Matching SOX: partner proteins and co-factors of the SOX family of transcriptional regulators. Curr. Opin. Genet. Dev. 12:441-446.
50. Wissmüller, S., T. Kosian, M. Wolf, M. Finzsch, and M. Wegner. 2006. The high-mobility-group domain of Sox proteins interacts with DNA-binding domains of many transcription factors. Nucleic Acids Res. 34:1735-1744.
51. Wrabetz, L., M. L. Feltri, K. A. Kleopa, and S. S. Scherer. 2004. Inherited neuropathies: clinical, genetic and biological features, p. 905-951. In R. A. Lazzarini (ed.), Myelin biology and disorders. Elsevier Academic Press, San Diego, CA.
52. Zorick, T. S., D. E. Syroid, E. Arroyo, S. S. Scherer, and G. Lemke. 1996. The transcription factors SCIP and Krox-20 mark distinct stages and cell fates in Schwann cell differentiation. Mol. Cell. Neurosci. 8:129-145.
53. Zorick, T. S., D. E. Syroid, A. Brown, T. Gridley, and G. Lemke. 1999. Krox-20 controls SCIP expression, cell cycle exit and susceptibility to apoptosis in developing myelinating Schwann cells. Development 126:1397-1406.