Differential regulation of the zinc finger genes Krox-20 and Krox-24 (Egr-1) suggests antagonistic roles in Schwann cells

Journal of Neuroscience Research

Volumn 50, Issue 5, 1997, Pages 702-712

  Topilko, Piotr ^a   Levi, Giovanni ^a,b   Merlo, Giorgio ^b   Mantero, Stefano ^b   Desmarquet, Carole ^a   Mancardi, Gianluigi ^c   Charnay, Patrick ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

Author keywords

Demyelinating neuropathies; Nerve regeneration; Peripheral nerve; Schwann cell development

Indexed keywords

ZINC FINGER PROTEIN;

ANIMAL TISSUE; ARTICLE; DEMYELINATING DISEASE; DNA SEQUENCE; GENE CONTROL; GENE EXPRESSION; MOUSE; MYELINATION; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; SCHWANN CELL;

ANIMALS; DNA-BINDING PROTEINS; EARLY GROWTH RESPONSE PROTEIN 1; EARLY GROWTH RESPONSE PROTEIN 2; EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMEDIATE-EARLY PROTEINS; MICE; MYELIN SHEATH; NERVOUS SYSTEM DISEASES; SCHWANN CELLS; SCIATIC NERVE; STEM CELLS; SURAL NERVE; TRANSCRIPTION FACTORS; ZINC FINGERS;

EID: 0030696010     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19971201)50:5<702::AID-JNR7>3.0.CO;2-L     Document Type: Article

References (52)

1. Aguayo AJ, Epps J, Charron L, Bray GM (1976): Multipotentiality of Schwann cells in cross-anastomosed and grafted myelinated and unmyelinated nerves: Quantitative microscopy and radioautography. Brain Res 104:1-20.
2. Archelos JJ, Roggenhuck K, Sehneider-Sehaulies J, Linington C, Tovka KV, Hartung H-P (1993): Production and characterisation of monoclonal antibodies to the extracellular domain of P0. J Neurosci Res 35:46-53.
3. Blanchard A, Sinanan A, Parmantier E, Zwart R, Broos L, Meijer D, Meier C, Jessen K, Mirsky R (1996): Oct6 (SCIP/Tst-1) is expressed in Schwann cell precursors, emhryonic Schwann cells, and postnatal myelinating Schwann cells: Comparison with Oct-1, Krox-20, and Pax-3. J Neurosci Res 46:630-640.
4. Brunden KR, Windebank AJ, Poduslo JF (1990): Role of axons in the regulation of P0 biosynthesis by Schwann cells. J Neurosci 26:135-143.
5. Cao XM, Koski RA, Cashler A, McKiernan M, Morris CF, Gaffney R, Hay RV, Sukhatme VP (1990): Identification and characterization of the Egr-1 gene product, a DNA-binding zinc finger protein induced by differentiation and growth signals. Mol Cell Biol 10:1931-1939.
6. Chavrier P, Zerial M, Lemaire P, Almendral J, Bravo R, Charnay P (1988): A gene encoding a protein with zinc fingers is activated during G0/G1 transition in cultured cells. EMBO J 7:29-35.
7. Chavrier P, Vesque C, Galliot B, Vigneron M, Dollé P, Duboule D, Charnay P (1990): The segment-specific gene Krox-20 encodes a transcription factor with binding sites in the promoter region of the Hox-1.4 gene. EMBO J 9:1209-1218.
8. Christy BA, Nathans D (1989): DNA-binding site of the growth factor-inducible protein Zif268. Proc Natl Acad Sci USA 86:8737-8741.
9. Christy BA, Lau LF, Nathans D (1988): A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with "zinc finger" sequences. Proc Natl Acad Sci USA 85:7857-7861.
10. Dong Z, Brennan A, Liu N, Yarden Y, Lefkowitz G, Mirsky R, Jessen KR (1995): Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15:585-596.
11. Fawcett JW, Keynes RJ (1990): Peripheral nerve regeneration. Annu Rev Neurosci 13:43-60.
12. He X, Treacy MN, Simmons DM, Ingraham HA, Swanson LW, Rosenfeld MG (1989): Expression of a large family of POU-domain regulatory genes in mammalian brain development. Nature 340:35-41.
13. Jaegle M, Mandemakers W, Broos L, Zwart R, Karis A, Visser P, Grosveld F, Meijer D (1996): The POU factor Oct-6 and Schwann cell differentiation. Science 273:507-510.
14. Jessen KR, Mirsky R (1992): Schwann cells: Early lineage, regulation of proliferation and control of myelin formation. Curr Opin Neurobiol 2:575-581.
15. Jessen KR, Morgan L, Stewart HJ, Mirsky R (1990): Three markers of adult non-myelin-forming Schwann cells, 217c(Ran-1). A5E3 and GFAP: Development and regulation by neuron-Schwann cell interactions. Development 109:91-103.
16. Jessen KR, Brennan A, Morgan L, Mirsky R, Kent A, Hashimoto Y, Gavrilovic J (1994): The Schwann cell precursor and its fate: A study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron 12:509-527.
17. Kioussi C, Gross MK, Gruss P(1995): Pax3: A paired domain gene as a regulator in PNS myelination. Neuron 15:553-562.
18. Klüver H, Barrera E (1953): A method for the combined staining of cells and fibers in the nervous system. J Neuropathol Exp Neurol 12:400-403.
19. Lee SL, Sadovsky Y, Swirnoff AH, Polish JA, Goda P, Gavrilina G, Milbrandt J (1996): Luteinizing hormone deficiency and female infertility in mice lacking the transcription factor NGFI-A (Egr-1). Science 273:1219-1221.
20. Lemaire P, Revelant O, Bravo R, Charnay P (1988): Two genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cell. Proc Natl Acad Sci USA 85:4691-4695.
21. Lemaire P, Vesque C, Schmitt J, Stunnenberg H, Frank R, Charnay P (1990): The serum-inducible mouse gene Krox-24 encodes a sequence-specific transcriptional activator. Mol Cell Biol 10: 3456-3467.
22. Lemke G (1996): Neuregulins in development. Mol Cell Neurosci 7:247-262.
23. Lemke G, Chao M (1988): Axons regulate Schwann cell expression of the major myelin and NGF receptor genes. Development 102:499.
24. Levi G, Topilko P, Schneider-Maunoury S, Lasagna M, Mantero S, Cancedda R, Charnay P (1996): Defective bone formation in Krox-20 mutant mice. Development 122:113-120.
25. Mancardi GL, Cadoni A, Tabaton M, Schenone A, Zicca A, De Martini I, Bianchini D, Dainiani G, Zaccheo D (1991): Schwann cell GFAP expression increase in axonal neuropathies. J Neurol Sci 102:177-183.
26. Meijer D, Graus A, Kraay R, Langeveld A, Mulder MP, Grosveld G (1990): The octamer binding factor Oct6: cDNA cloning and expression in early embryonic cells. Nucleic Acids Res 18:7357-7365.
27. Milbrandt J (1987): A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238:797-799.
28. Moase CE, Trasler DG (1990): Delayed neural crest emigration from Sp and Sp delayed mouse neural tube explants. Teratology 42:171-182.
29. Monuki ES, Weinmaster G, Kuhn R, Lemke G (1989): SCIP: A glial POU domain gene regulated by cyclic AMP. Neuron 3:783-793.
30. Monuki ES, Kuhn R, Weinmaster G, Trapp BD, Lemke G (1990): Expression and activity of the POU transcription factor SCIP. Science 249:1300-1303.
31. Monuki ES, Kuhn R, Lemke G (1993): Repression of the myelin P0 gene by the POU transcription factor SCIP. Mech Dev 42:15-32.
32. Murphy P, Topilko P, Schneider-Maunoury S, Seitanidou T, Baron-Van Evercooren A, Charnay P (1996): The regulation of Krox-20 expression reveals important steps in the control of peripheral glial cell development. Development 122:2847-2857.
33. Nikam SS, Tennekoon GI, Christy BA, Yoshino JE, Rutkowski JL (1995): The zinc finger transcription factor Zif268/Egr-1 is essential for Schwann cell expression of the p75 NGF receptor. Mol Cell Neurosci 6:337-348.
34. Nonchev S, Vesque C, Maconochie M, Seitanidou T, Ariza-McNaughton L, Frain M, Marshall H, Sham MH, Krumlauf R, Charnay P (1996): Segmental expression of Hoxa-2 in the hindbrain is directly regulated by Krox-20. Development 122:543-554.
35. Pelligrino RG, Politis MJ, Ritchie JM, Spencer PS (1986): Events in degenerating cat peripheral nerve: Induction of Schwann cell S phase and its relation to nerve degeneration. J Neurocytol 15:17-28.
36. Russo MW, Sevetson BR, Milbrandt J (1995): Identification of NAB1, a repressor of NGFI-A and Krox-20-mediated transcription. Proc Natl Acad Sci USA 92:6873-6877.
37. Schneider-Maunoury S, Topilko P, Seitanidou T, Levi G, Cohen-Tannoudji M, Pournin S, Babinet C, Charnay P (1993): Disruption of Krox-20 results in alteration of rhombomeres 3 and 5 in the developing hindbrain. Cell 75:1199-1214.
38. Shah NM, Marchionni MA, Isaacs I, Stroobant P, Anderson DJ (1994): Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77:349-360.
39. Sham MH, Vesque C, Nonchev S, Marshall H, Frain M, Das Gupta R, Whiting J, Wilkinson D, Charnay P, Krumlauf R (1993): The zinc linger gene Krox20 regulates HoxB2 (Hox2.8) during hindbrain segmentation. Cell 72:183-196.
40. Sukhatme VP, Cao X, Chang LC, Tsai-Morris C-H, Stanienkovich D, Ferreira PCP, Cohen DR, Edwards SA, Shows TB, Curran T, Le Beau MM, Adamson ED (1988): A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization. Cell 53:37-43.
41. Suzuki N, Rohdewohld H, Neuman T, Gruss P, Scholer HR (1990): Oct-6: A POU transcription factor expressed in embryonal stem cells and in the developing brain. EMBO J 9:3723-3732.
42. Svaren J, Sevetson BR, Apel ED, Zimonjic DB, Popescu NC, Milbrandt J (1996): NAB2, a corepressor of NGFI-A (Egr-1) and Krox-20, is induced by proliferative and differentiative stimuli. Mol Cell Biol 16:3545-3553.
43. Swirnoff AH, Milbrandt J (1995): DNA-binding specificity of NGFI-A and related zinc finger transcription factors. Mol Cell Biol 15:2275-2287.
44. Topilko P, Schneider-Maunoury S, Levi G, Baron-Van Evercooren A, Chennoufi ABY, Seitanidou T, Babinet C, Charnay P (1994): Krox-20 controls myelination in the peripheral nervous system. Nature 371:796-799.
45. Topilko P, Murphy P, Charnay P (1996): Embryonic development of Schwann cells: Multiple roles for neuregulins along the pathway. Mol Cell Neurosci 8:71-75.
46. Topilko P, Schneider-Maunoury S, Goi G, Trembleau A, Gourdji D, Du'ancourt MA, Rao CV, Charnay P (1997): Multiple pituitary and ovarian defects in Krox-24 (NGFI-A, Eg2-1) targeted mice. Mol Endocrinol (in press).
47. Trapp BD, Hauer P, Lemke G (1988): Axonal regulation of myelin protein mRNA levels in actively myelinating Schwann cells. J Neurosci 8:3515.
48. Vandromme M, Gauthier-Rouvière C, Lamb N, Fernandez A (1996): Regulation of transcription factor localization: Fine-tuning of gene expression. Trends Biochem Sci 21:59-64.
49. Vesque C, Charnay P (1992): Mapping functional regions of the segment-specific transcription factor Krox-20. Nucleic Acids Res 20:2485-2492.
50. Watson MA, Milbrandt J (1990): Expression of the nerve growth factor-regulated NGFI-A and NGFI-B genes in the developing rat. Development 110:173-183.
51. Weinstein DE, Burrola PG, Lemke G (1995): Premature Schwann cell differentiation and hypermyelination in mice expressing a targeted antagonist of the POU transcription factor SCIP. Mol Cell Neurosci 6:212-229.
52. Whiteside ST, Goodbourn S (1993): Signal transduction and nuclear targeting: Regulation of transcription factor activity by subcellular localisation. J Cell Sci 104:949-955.