Intracellular events mediating insulin-like growth factor I-induced oligodendrocyte development: Modulation by cyclic AMP

Journal of Neurochemistry

Volumn 95, Issue 4, 2005, Pages 1091-1107

  Palacios, Nuria ^a   Sánchez Franco, Franco ^b   Fernández, Miriam ^a   Sánchez, Isabel ^a   Cacicedo, Lucinda ^a  

^a HOSPITAL RAMÓN Y CAJAL   (Spain)

^b HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

Author keywords

Cyclic AMP; Cyclic AMP response element binding protein; Insulin like growth factor I; Mitogen activated protein kinase; Oligodendrocytes; Phosphatidylinositol 3 kinase

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL CULTURE; CELL TYPE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; MYELINATION; NERVE CELL DIFFERENTIATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBELLAR CORTEX; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DRUG INTERACTIONS; EMBRYO; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR I; INTRACELLULAR SPACE; MODELS, BIOLOGICAL; MYELIN BASIC PROTEINS; OLIGODENDROGLIA; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; TUBULIN;

ANIMALIA;

EID: 28244443656     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03419.x     Document Type: Article

References (89)

1. Afshari F. S., Chu A. K. and Sato-Bigee C. (2001) Effect of cyclic AMP on the expression of myelin basic protein species and myelin proteolipid protein in committed oligodendrocytes: differential involvement of the transcription factor CREB. J. Neurosci. Res. 66, 37-45.
2. Alarcón-Segovia D., Ruiz-Argüelles A. and Fishbein E. (1978) Antibody to nuclear ribonucleoprotein penetrates live human mononuclear cells through Fc receptors. Nature 261, 67-69.
3. Alarcón-Segovia D., Ruiz-Argüelles A. and Llorente L. (1996) Broken dogma: penetration of autoantibodies into living cells. Immunol. Today 17, 163-164.
4. Alessi D. R., James S. R., Downes C. P., Holmes A. B., Gaffney P. R. J., Reese C. B. and Cohen P. (1997) Characterization of a 3-phosphoinositide- dependent protein kinase which phosphorylates and activates protein kinase B α. Curr. Biol. 7, 261-269.
5. Anderson S. and Miskimins R. (1994) Involvement of protein kinase C in cAMP regulation of myelin basic protein gene expression. J. Neurosci. Res. 37, 604-611.
6. Backer J. M., Myers M. G. Jr, Sun X. J., Chin D. J., Shoelson S. E., Miralpeix M. and White M. F. (1993) Association of IRS-1 with the insulin receptor and the phosphatidylinositol 3′-kinase. Formation of binary and ternary signaling complexes in intact cells. J. Biol. Chem. 268, 8204-8212.
7. Baron-Van Evercooren A., Olichon-Berthe C., Kowalski A., Visciano G. and Van Obberghen E. (1991) Expression of IGF-I and insulin receptor genes in the rat central nervous system: a developmental, regional and cellular analysis. J. Neurosci. Res. 28, 144-253.
8. Barres B. A., Hart I. K., Coles H. S. R., Burne J. F., Voyvodic J. T., Richardson W. D. and Raff M. C. (1992) Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31-46.
9. Barres B. A., Schmid R., Sendtner M. and Raff M, C. (1993) Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118, 282-295.
10. Barres B. A., Raff M. C., Gaese F., Bartke I., DeChant G. and Barde Y. A. (1994) A crucial role for neurotrophin-3 in oligodendrocyte development. Nature 367, 371-375.
11. Beck K. D., Powell-Braxton L., Widmer H. R., Valverde J. and Hefti F. (1995) Igf-1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal and striatal parvalbumin-containing neurons. Neuron 14, 717-730.
12. Bradford M. M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 72, 248-254.
13. Burgering B. M. T., Pronk G. J., van Weeren P. C., Chardin P. and Bos J. L. (1993) cAMP antagonizes p21ras-directed activation of extracellular signal-regulated kinase 2 and phosphorylation of mSos nucleotide exchange factor. EMBO J. 12, 4211-4220.
14. Burlet A. J., Leon-Henri B. P., Robert F. R., Arahmani A., Fernette B. M. L. and Burlet C. R. (1987) Monoclonal anti-vasopressin (VP) antibodies penetrate into VP neurons in vivo. Exp. Brain Res. 65, 629-638.
15. Buscà R., Abbe P., Mantoux F., Aberdam E., Peyssonnaux C., Eychène A., Ortonne J. P. and Balloti R. (2000) Ras mediates the cAMP-dependent activation of extracellular signal-regulated kinases (ERKs) in melanocytes. EMBO J. 19, 2900-2910.
16. Canoll P. D., Musacchio J. M., Ardí R., Reynols R., Marchionni M. A. and Salzer J. L. (1996) GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 17, 229-243.
17. Carson M. J., Behringer R. R., Brinster R. L. and McMorris F. A. (1993) Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice. Neuron 10, 729-740.
18. Deng S. X., Hanson E. and Sanz I. (2000) In vivo cell penetration and intracellular transport of anti-Sm and anti-La autoantibodies. Inter. Immunol. 12, 415-423.
19. De Rooij J., Zwartkruis F. J. T., Verheijen M. H. G., Cool R. H., Nijman S. M. B., Wittinghofer A. and Bos J. L. (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396, 474-477.
20. Fang X., Yu S. X., Lu Y., Bast R. C. Jr, Woodgett J. R. and Mills G. B. (2000) Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc. Natl Acad. Sci. USA 97, 11 960-11 965.
21. Fratantoni S. A., Dubrovsky A. L. and Uchitel O. D. (1996) Uptake of immunoglobulin G from amyotrophic lateral sclerosis patients by motor nerve terminals in mice. J. Neurol. Sci. 137, 97-102.
22. Frödin M., Peraldi P. and Van Obberghen E. (1994) Cyclic AMP activates de mitogen-activated protein kinase cascade in PC 12 cells. J. Biol. Chem. 269, 6207-6214.
23. Fruttiger M., Karlsson L., Hall A. C. et al. (1999) Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development 126, 457-467.
24. Gandelman K. Y., Pfeiffer S. E. and Carson J. H. (1989) Cyclic AMP regulation of P0 and myelin basic protein gene expression in semidifferentiated peripheral neurinoma cell line D6P2T. Development 106, 389-398.
25. Ginty D. D., Bonni A. and Greenberg M. E. (1994) Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77, 713-725.
26. Gonzalez-Robayna I. J., Falender A. E., Ochsner S., Firestone G. L. and Richards J. S. (2000) FSH stimulates phosphorylation and activation of protein kinase B (PKB/Akt) and serum and glucocorticoidinduced kinase (Sgk): evidence for A-kinase independent signalling in ganulosa cells. Mol. Endocrinol 14, 1283-1300.
27. Graves L. M., Bornfeldt K. E., Raines E. W., Potts B. C., Macdonald S. G., Ross R. and Krebs E. G. (1993) Protein kinase A antagonizes platelet-derived growth factor-induced signalling by mitogen-activated protein kinase in human arterial smooth muscle cells. Proc. Natl Acad. Sci. USA 90, 10 300-10 304.
28. Grewal S. S., Fass D. M., Yao H., Elling C. L., Goodmand R. H. and Stork P J. S. (2000) Calcium and cAMP signals differentially regulate cAMP-responsive element binding protein function via a Rap1-extracellular signal-regulated kinase pathway. J. Biol. Chem. 275, 34433-34441.
29. Hu Q., Klippel A., Muslin A. J., Fantl W. J. and Williams L. T. (1995) Ras-dependent induction of cellular responses by constitutively active phosphatidylinositol-3 kinase. Science 268, 100-102.
30. Hwang O. and Choi H. J. (1995) Induction of gene expression of the catecholamine-synthesizing enzymes by insulin-like growth factor-I. J. Neurochem. 65, 1988-1996.
31. Izumi T., White M. F., Kadowaki T., Takaku F., Akanuma Y. and Kasuga M. (1987) Insulin-like growth factor I rapidly stimulates tyrosine phosphorylation of a Mr 185,000 protein in intact cells. J. Biol. Chem. 262, 1282-1287.
32. Jensen N. A., Smith G. M., Garvey J. S., Shine H. D. and Hood L. (1993) Cyclic AMP has a differentiative effect on an immortalized oligodendrocyte cell line. J. Neurosci. Res. 35, 288-296.
33. Kauffmann-Zeh A., Rodriguez-Viciana P., Ulrich E., Gilbert C., Coffer P., Downward J. and Evan G. (1997) Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature 385, 544-548.
34. Kawasaki H., Springett G. M., Mochizuki N., Toki S., Nakaya M., Matsuda M., Housman D. E. and Graybiel A. M. (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282, 2275-2279.
35. Kievit P., Lauten J. D. and Maurer R. A. (2001) Analysis of the role of the mitogenic-activated protein kinase in mediating cyclic-adenosine 3′-5′-monophosphate effects on prolactin promoter activity. Mol. Endocrinol. 15, 614-624.
36. Klippel A., Reinhard C., Kavanaugh W. M., Apell G., Escobedo M. A. and Williams L. T. (1996) Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol. Cell Biol. 16, 4117-4127.
37. Koscec M., Koren E., Wolfson-Reichlin M., Fugate R. D., Trieu E., Targoff I. N. and Reichlin M. (1997) Autoantibodies to ribosomal P proteins penetrate into live hepatocytes and cause cellular dysfunction in culture. J. Immunol. 159, 2033-2041.
38. Kyriakis J. M., App H., Zhang X.-F., Barnerjee P, Brautigam D. L., Rapp U. and Avruch J. (1992) Raf-1 activates MAP kinase kinase. Nature 358, 417-421.
39. Lee K. H., Calikoglu A. S., Ye P. and D'Ercole A. J. (1999) Insulin-like growth factor-I (IGF-I) ameliorates and Igf-I binding protein-1 (IGFBP-1) exacerbates the effects of undernutrition on brain growth during early postnatal life: studies in IGF-I and IGFBP-1 transgenic mice. Pediatr. Res. 45, 331-336.
40. MAPK cascade. J. Biol. Chem. 273, 32 400-32 407.
41. Liu H., Kublaoui B., Pilch P. F. and Lee J. (2000) Insulin activation of mitogen-activated protein (MAP) kinase and Akt is phosphatidylinositol 3-kinase-dependent in rat adipocytes. Biochem. Biophys. Res. Commun. 274, 845-851.
42. Liu W., Chin-Chance C., Lee E. J. and Lowe W. L. Jr (2002) Activation of phosphatidylinositol 3-kinase contributes to insulin-like growth factor I-mediated inhibition of pancreatic beta-cell death. Endocrinology 143, 3802-3812.
43. Ma J., Chapman G. V., Chen S. L., Melick G., Penny R. and Breit S. N. (1991) Antibody penetration of viable human cells I. Increased penetration of human lymphocytes by anti-RNP IgG. Clin. Exp. Immunol. 84, 83-91.
44. Mason J. L., Ye P., Suzuki K., D'Ercole A. J. and Matsushima G. K. (2000) Insulin-like growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J. Neurosci. 20, 5703-5708.
45. Mason J. L., Xuang S., Dragatsis I., Efstradiatis A. and Goldman J. E. (2003) Insulin-like growth factor (IGF) signaling through type 1 IGF receptor plays an important role in remyelination. J. Neurosci. 23, 7710-7718.
46. Masters B. A., Werner H., Roberts C. T. Jr, LeRoih D. and Raizada M. K. (1991) Insulin-like growth factor I (IGF-I) receptors and IGF-I actions in oligodendrocytes from rat brains. Regul. Pept. 33, 117-131.
47. McMorris F. A. (1983) Cyclic AMP induction of the myelin enzyme 2′,3′-cyclic nucleotide 3′-phosphohydrolase in rat oligodendrocytes. J. Neurochem. 41, 121-132.
48. McMorris F. A. and Dubois-Dalcq M. (1988) Insulin-like growth factor I promotes cell proliferation and oligodendroglial commitment in rat glial progenitors cell developing in vitro. J. Neurosci. Res. 21, 199-209.
49. McMorris F. A., Smith T. M., DeSalvo S. and Furlanetto R. W. (1986) Insulin-like growth factor I/somatomedin C: a potent inducer of oligodendrocyte development. Proc. Natl Acad. Sci. USA 83, 822-826.
50. McMorris F. A., Furlanetto R. W., Mozell R. L., Carson M. J. and Raible D. W. (1990) Regulation of oligodendrocyte development by insulin growth factors and cyclic nucleotides. Ann. NY Acad. Sci. 605, 101-109.
51. Mehrhof F. B., Muller F. U., Bergmann M. W., Li P., Wang Y., Schmitz W., Dietz R. and von Harsdorf R. (2001) In cardiomyocyte hypoxia, insulin-like growth factor-I-induced antiapoptotic signalling requires phosphatidylinositol- 3-OH-kinase-dependent and mitogen-activated protein kinase-dependent activation of the transcription factor cAMP response element-binding protein. Circulation 104, 2088-2094.
52. Mohamed H. A., Mosier D. R., Zou L. L., Siklos L., Alexianu M. E., Engelhardt J. L., Beers D. R., Le W. D. and Appel S. H. (2002) Immunoglobulin Fc gamma receptor promotes immunoglobulin uptake, immunoglobulin-mediated calcium increase, and neuro-transmitter release in motor neurons. J. Neurosci. Res. 69, 110-116.
53. Moodie S. A., Willumsen B. M., Weber M. J. and Wolfman A. (1993) Complexes of Ras.GTP with Raf-1 and mitogen-activated protein kinase kinase. Science 260, 1658-1661.
54. Mozell R. L. and McMorris F. A. (1991) Insulin-like growth factor I stimulates oligodendrocyte development and myelination in rat brain aggregate cultures. J. Neurosci. Res. 30, 382-390.
55. Myers M. G., Backer J. M., Sun X.-J., Shoelson S. E., Hu P., Schlessinger J., Yoakin M., Schaffnausen B. and White M. E. (1992) IRS-1 activates the phosphatidylinositol 3′-kinase by associating with the Src homology 2 domains of p85. PNAS 89, 10 350-10 354.
56. Payne D. M., Rossomando A. J., Martino P., Erickson A. K., Her J. H., Shabanowitz J., Hunt D. F., Weber M. J. and Sturgill T. W. (1991) Identification of the regulatory phosphorylation sites in pp42/mitogen-activated protein kinase (MAP kinase). EMBO J. 10, 885-892.
57. Pugazhenthi S., Boras T., O'Connor D., Meintzer M. K., Heindenreich K. A. and Reusch J. E. (1999) Insulin-like growth factor I-mediated activation of the transcription factor cAMP response element-binding protein in PC12 cells. Involvement of p38 mitogen-activated protein kinase-mediated pathway. J. Biol. Chem. 274, 2829-2837.
58. Raff M. C., Miller R. H. and Noble M. (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 390-396.
59. Raible D. W. and McMorris F. A. (1989) Cyclic AMP regulates the rate of differentiation of oligodendrocytes without changing the lineage commitment of their progenitors. Dev. Biol. 133, 437-466.
60. Raible D. W. and McMorris F. A. (1990) Induction of oligodendrocyte differentiation by activators of adenylate cyclase. J. Neurosci. Res. 27, 43-46.
61. Raible D. W. and McMorris F. A. (1993) Oligodendrocyte differentiation and progenitor cell proliferation are independently regulated by cyclic AMP. J. Neurosci. Res. 34, 287-294.
62. Rehmann H., Schwede F., Deskeland S. O., Wittinghofer A. and Boss J. L. (2003) Ligand-mediated activation of the cAMP-responsive guanine nucleotide exchange factor Epac. J. Biol. Chem. 278, 38 548-38 556.
63. Richards J. (2001) New signalling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol. Endocrinol. 15, 209-218.
64. Richardson W. D., Pringle N., Mosley M. J., Westermark B. and Dubois-Dalcq M. (1988) A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell 53, 309-319.
65. Saneto R. P., Low K. G., Melner M. H. and De Vellis J. (1988) Insulin/insulin-like growth factor I and other epigenetic modulators of myelin basic protein expression in isolated oligodendrocyte progenitors cells. J. Neurosci. Res. 21, 210-219.
66. Sato-Bigbee C. and Yu R. K. (1993) Presence of a cAMP response element binding protein in oligodendrocytes. J. Neurochem. 60, 2106-2110.
67. Sato-Bigbee C. and De Vries G. H. (1996) Treatment of oligodendrocytes with antisense deoxyoligonucleotide directed against CREB mRNA: Effect on the cyclic-dependent induction of myelin basic protein expression. J. Neurosci. Res. 46, 98-107.
68. Sato-Bigbee C., Chan E. L. P. and Yu R. K. (1994) Oligodendroglial cyclic AMP response element-binding protein: a member of the CREB family of transcription factors. J. Neurosci. Res. 38, 621-628.
69. Schmitt J. M. and Stork P. J. S. (2001) Cyclic AMP-mediated inhibition of cell growth requires the small G protein Rap1. Mol. Cell Biol. 21, 3671-3683.
70. Sevetson B. R., Kong X. and Lawrence J. C. J. (1993) Increasing cAMP attenuates activation of mitogen-activated protein kinase. Proc. Natl Acad. Sci. USA 90, 10 305-10 309.
71. Shemer J., Raizada M. K., Masters B. A., Ota A. and LeRoith D. (1987) Insulin-like growth factor I receptors in neuronal and glial cells. J. Biol. Chem. 262, 763-769.
72. Skolnik E. Y., Batzer A., Li N., Lee C. H., Lowenstein F., Mohammadi M., Margolis B. and Schlessinger J. (1993a) The function of GRB2 in linking the insulin receptor to Ras signaling pathways. Science 260, 1953-1955.
73. Skolnik E. Y., Lee C. H., Batzer A. et al. (1993b) The SH2/SH3 domain-containing protein GRB2 interacts with tyrosine-phosphorylated IRS1 and She: implications for insulin control of ras signalling. EMBO J. 12, 1929-1936.
74. Skopura A. F. and McMorris F. A. (1995) Cyclic AMP regulates messenger RNA for myelin proteins in developing oligodendrocytes in both positive and negative fashions. J. Neurochem. 64, S47B.
75. Stork P. J. S. and Schmitt J. M. (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. TRENDS Cell. Biol. 12, 258-266.
76. Studzinski D. M., Ramaswamy R. and Benjamins J. A. (1998) Effects of cyclic AMP on expression of myelin genes in the N20.1 oligodendroglial cell line. Neurochem. Res. 23, 435-441.
77. Van der Paal R. H. M., Koper J. W., Van Golde L. M. G. and Lopez-Cardozo M. (1988) Effects of insulin and insulin-like growth factor I (IGF-I) on oligodendrocyte-enriched glial cultures. J. Neurosci. Res. 19, 483-490.
78. Vemuri G. S. and McMorris F. A. (1996) Oligodendrocytes and their precursors require phosphatidylinositol 3-kinase signaling for survival. Development 122, 2529-2537.
79. Vlahos C. J., Matter W. F., Hui K. Y. and Brown R. F. (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(-4-morpholinyl)-8-phenyl-4H-1- benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248.
80. Vossler M. R., Yao H., York R. D., Pan M. G., Rim C. S. and Stork P. J. S. (1997) cAMP activates MAP kinase and Elk-1 through a B-Raf and Rap1-dependent pathway. Cell 89, 73-82.
81. Wang L., Liu F. and Adamo M. L. (2001 ) Cyclic AMP inhibits extracellular signal-regulated kinase and phosphatidylinositol 3-kinase/Akt pathways by inhibiting Rap 1. J. Biol. Chem. 276, 37 242-37 249.
82. Wood K., Sarnecki C., Roberts T. M. and Blenis J. (1992) Ras mediates nerve growth factor receptor modulation of three signal-transducing protein kinases: MAP kinase, Raf-1 and RSK. Cell 68, 1041-1050.
83. Xing J., Ginty D. D. and Greenberg M. E. (1996) Coupling of the Ras-MAPK pathways to gene activation by RSK 2, a growth factor-regulated CREB kinase. Science 273, 959-963.
84. Yamada M., Tanabe K., Wada K., Shimoke K., Ishikawa Y., Ikeuchi T., Koizumi S. and Hatanaka H. (2001) Differences in survival-promoting effects and intracellular signaling properties of BDNF and IGF-I in cultured cortical neurons. J. Neurochem. 78, 940-951.
85. Yao D. L., West N. R., Bondy C. A., Brenner M., Hudson L. D., Zhou J., Collins G. H. and Webster H. F. (1995) Cryogenic spinal cord injury induces astrocytic gene expression of insulin-like growth factor I and insulin-like growth factor binding protein 2 during myelin regeneration. J. Neurosci. Res. 40, 647-659.
86. Ye P., Carson J. and D'Ercole A. J. (1995) In vivo actions of insulin-like growth factor-I (IGF-I) on brain myelination: studies of IGF-I and IGF binding protein-1 (IGFBP-1) transgenic mice. J. Neurosci. 15, 7344-7356.
87. Ye P., Lee K. H. and D'Ercole A. J. (2000) Insulin-like growth factor I (IGF-I) protects myelination from undernutritional insult: studies of transgenic mice overexpressing IGF-I in brain. J. Neurosci. Res. 62, 700-708.
88. Yonehara T., Kanasaki H., Yamamoto H., Fukunaga K., Miyazaki K. and Miyamoto E. (2001) Involvement of mitogen-activated protein kinase in cyclic adenosine 3′-5′-monophosphate-induced hormone gene expression in rat pituitary GH3 cells. Endocrinology 142, 2811-2819.
89. Zhang X. and Miskimins R. (1993) Binding at an NFI site is modulated by cAMP-dependent activation of myelin basic protein gene expression. J. Neurochem. 60, 2010-2017.