The basic region and leucine zipper transcription factor MafK is a new nerve growth factor-responsive immediate early gene that regulates neurite outgrowth

Journal of Neuroscience

Volumn 22, Issue 20, 2002, Pages 8971-8980

  Töröcsik, Béata ^a,b,c   Angelastro, James M ^a   Greene, Lloyd A ^a  

^a Columbia Univ Coll of Phys/Surg ^*  (United States)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c UNIVERSITY OF PÉCS   (Hungary)

Author keywords

Differentiation; Immediate early gene; MafK; NGF; PC12 cell; Transcription factor

Indexed keywords

CYCLIC AMP DERIVATIVE; EPIDERMAL GROWTH FACTOR; LEUCINE ZIPPER PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE C; RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MAFG; TRANSCRIPTION FACTOR MAFK; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRAIN; DEPOLARIZATION; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; IMMEDIATE EARLY GENE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; TELENCEPHALON;

EID: 0037109676     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-20-08971.2002     Document Type: Article

References (72)

1. Angelastro JM, Klimaschewski L, Tang S, Vitolo OV, Weissman TA, Donlin LT, Shelanski ML, Greene LA (2000) Identification of diverse nerve growth factor-regulated genes by serial analysis of gene expression (SAGE) profiling. Proc Natl Acad Sci USA 97:10424-10429.
2. Angelastro JM, Moon NY, Liu DX, Yang AS, Greene LA, Franke TF (2001) Characterization of a novel isoform of caspase-9 that inhibits apoptosis. J Biol Chem 276:12190-12200.
3. Bartel DP, Sheng M, Lau LF, Greenberg ME (1989) Growth factors and membrane depolarization activate distinct programs of early response gene expression: Dissociation of fos and jun induction. Genes Dev 3:304-313.
4. Blank V, Kim MJ, Andrews NC (1997) Human MafG is a functional partner for p45 NF-E2 in activating globin gene expression. Blood 89:3925-3935.
5. Bleasdale JE, Bundy GL, Bunting S, Fitzpatrick FA, Huff RM, Sun FF, Pike JE (1989) Inhibition of phospholipase C dependent processes by U-73, 122. Adv Prostaglandin Thromboxane Leukot Res 19:590-593.
6. Burstein DE, Blumberg PM, Greene LA (1982) Nerve growth factor-induced neuronal differentiation of PC12 pheochromocytoma cells: Lack of inhibition by a tumor promoter. Brain Res 247:115-119.
7. Coleman ES, Wooten MW (1994) Nerve growth factor-induced differentiation of PC12 cells employs the PMA-insensitive protein kinase C-zeta isoform. J Mol Neurosci 5:39-57.
8. Curran T, Morgan JI (1985) Superinduction of c-fos by nerve growth factor in the presence of peripherally active benzodiazepines. Science 229:1265-1268.
9. Douglas DN, Fink HS, Ridgway ND, Cook HW, Byers DM (1999) Myristoylated alanine-rich C-kinase substrate is phosphorylated and translocated by a phorbol ester-insensitive and calcium-independent protein kinase C isoform in C6 glioma cell membranes. Biochim Biophys Acta 1448:439-449.
10. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
11. Farias-Eisner R, Vician L, Silver A, Reddy S, Rabbani SA, Herschman HR (2000) The urokinase plasminogen activator receptor (UPAR) is preferentially induced by nerve growth factor in PC12 pheochromocytoma cells and is required for NGF-driven differentiation. J Neurosci 20:230-239.
12. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F, Copeland RA, Magolda RL, Scherle PA, Trzaskos JM (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273:18623-18632.
13. Friedman WJ, Greene LA (1999) Neurotrophin signaling via Trks and p75. Exp Cell Res 253:131-142.
14. Fujiwara KT, Kataoka K, Nishizawa M (1993) Two new members of the maf oncogene family, mafK, and mafF, encode nuclear b-Zip proteins lacking putative trans-activator domain. Oncogene 8:2371-2380.
15. Gerstin Jr EH, McMahon T, Dadgar J, Messing RO (1998) Protein kinase C delta mediates ethanol-induced up-regulation of L-type calcium channels. J Biol Chem 273:16409-16414.
16. Gschwendt M, Dietrich S, Rennecke J, Kittstein W, Müller H-J, Johannes F-J (1996) Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase c isoenzymes. FEBS Lett 392:77-80.
17. Greenberg ME, Greene LA, Ziff EB (1985) Nerve growth factor and epidermal growth factor induce rapid transient changes in protooncogene transcription in PC12 cells. J Biol Chem 260:14101-14110.
18. Greene LA, Kaplan DR (1995) Early events in neurotrophin signalling via Trk and p75 receptors. Curr Opin Neurobiol 5:579-587.
19. Greene LA, Tischler AS (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73:2424-2428.
20. Greene LA, Burstein DE, Black MM (1982) The role of transcription-dependent priming in nerve growth factor promoted neurite outgrowth. Dev Biol 91:305-316.
21. Greene LA, Farinelli SE, Cunningham ME, Park DS (1998) Culture and experimental use of the PC12 rat pheochromocytoma cell line. In: Culturing Nerve Cells (Banker G, Goslin K, eds), Ed 2, pp 161-188. Cambridge MA: MIT.
22. Hall FL, Fernyhough P, Ishii DN, Vulliet PR (1988) Suppression of nerve growth factor-directed neurite outgrowth in PC12 cells by sphingosine, an inhibitor of protein kinase C. J Biol Chem 263:4460-4466.
23. Herschman HR (1991) Primary response genes induced by growth factors and tumor promoters. Annu Rev Biochem 60:281-319.
24. Hill CS, Treisman R (1995) Transcriptional regulation by extracellular signals: Mechanisms and specificity. Cell 80:199-211.
25. Kaplan DR, Miller FD (2000) Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10:381-391.
26. Kaplan MP, Chin SS, Macioce P, Srinawasan J, Hashim G, Liem RK (1991) Characterization of a panel of neurofilament antibodies recognizing N-terminal epitopes. J Neurosci Res 30:545-554.
27. Katsuoka F, Motohashi H, Onodera K, Suwabe N, Engel JD, Yamamoto M (2000) One enhancer mediates mafK transcriptional activation in both hematopoietic and cardiac muscle cells. EMBO J 19:2980-2991.
28. Kotkow KJ, Orkin SH (1995) Dependence of globin gene expression in mouse erythroleukemia cells on the NF-E2 heterodimer. Mol Cell Biol 15:4640-4647.
29. Kotkow KJ, Orkin SH (1996) Complexity of the erythroid transcription factor NF-E2 as revealed by gene targeting of the mouse p18 NF-E2 locus. Proc Natl Acad Sci USA 93:3514-3518.
30. Laywell ED, Kukekov VG, Steindler DA (1999) Multipotent neurospheres can be derived from forebrain subependymal zone and spinal cord of adult mice after protracted postmortem intervals. Exp Neurol 156:430-433.
31. Leonard DG, Ziff EB, Greene LA (1987) Identification and characterization of mRNAs regulated by nerve growth factor in PC12 cells. Mol Cell Biol 7:3156-3167.
32. Lessard JL (1988) Two monoclonal antibodies to actin: One muscle selective and one generally reactive. Cell Motil Cytoskeleton 10:349-362.
33. Levkovitz Y, O'Donovan KJ, Baraban JM (2001) Blockade of NGF-induced neurite outgrowth by a dominant-negative inhibitor of the egr family of transcription regulatory factors. J Neurosci 21:45-52.
34. Li W, Cogswell CA, LoTurco JJ (1998) Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J Neurosci 18:8853-8862.
35. Marshall CJ (1995) Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
36. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, Hug H, Marme D, Schachtele C (1993) Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J Biol Chem 268:9194-9197.
37. Milbrandt J (1987) A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238:797-799.
38. Milbrandt J (1988) Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron 1:183-188.
39. Moscat J, Diaz-Meco MT (2000) The atypical protein kinase Cs. Functional specificity mediated by specific protein adapters. EMBO Rep 1:399-403.
40. Motohashi H, Igarashi K, Onodera K, Takahashi S, Ohtani H, Nakafuku M, Nishizawa M, Engel JD, Yamamoto M (1996) Mesodermal- vs. neuronal-specific expression of MafK is elicited by different promoters. Genes Cells 1:223-238.
41. Motohashi H, Shavit JA, Igarashi K, Yamamoto M, Engel JD (1997) The world according to Maf. Nucleic Acids Res 25:2953-2959.
42. Motohashi H, Ohta J, Engel JD, Yamamoto M (1998) A core region of the mafk gene IN promoter directs neurone-specific transcription in vivo. Genes Cells 3:671-684.
43. Motohashi H, Katsuoka F, Shavit JA, Engel JD, Yamamoto M (2000) Positive or negative MARE-dependent transcriptional regulation is determined by the abundance of small Maf proteins. Cell 103:865-875.
44. Nishizawa M, Kataoka K, Goto N, Fujiwara KT, Kawai S (1989) v-maf, a viral oncogene that encodes a "leucine zipper" motif. Proc Natl Acad Sci USA 86:7711-7715.
45. Onodera K, Shavit JA, Motohashi H, Yamamoto M, Engel JD (2000) Perinatal synthetic lethality and hematopoietic defects in compound mafG::mafK mutant mice. EMBO J 19:1335-1345.
46. Peng X, Greene LA, Kaplan DR, Stephens RM (1995) Deletion of a conserved juxtamembrane sequence in Trk abolishes NGF-promoted neuritogenesis. Neuron 15:395-406.
47. Qu Z, Wolfraim LA, Svaren J, Ehrengruber MU, Davidson N, Milbrandt J (1998) The transcriptional corepressor NAB2 inhibits NGF-induced differentiation of PC12 cells. J Cell Biol 142:1075-1082.
48. Quest AF (1996) Regulation of protein kinase C: A tale of lipids and proteins. Enzyme Protein 49:231-261.
49. Roivainen R, McMahon T, Messing RO (1993) Protein kinase C isozymes that mediate enhancement of neurite outgrowth by ethanol and phorbol esters in PC12 cells. Brain Res 624:85-93.
50. Sassone-Corsi P, Der CJ, Verma IM (1989) ras-induced neuronal differentiation of PC12 cells: Possible involvement of fos and jun. Mol Cell Biol 9:3174-3183.
51. Schlingensiepen KH, Wollnik F, Kunst M, Schlingensiepen R, Herdegen T, Brysch W (1994) The role of Jun transcription factor expression and phosphorylation in neuronal differentiation, neuronal cell death, and plastic adaptations in vivo. Cell Mol Neurobiol 14:487-505.
52. Segal RA, Greenberg ME (1996) Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci 19:463-489.
53. Shavit JA, Motohashi H, Onodera K, Akasaka J, Yamamoto M, Engel JD (1998) Impaired megakaryopoiesis and behavioral defects in mafG-null mutant mice. Genes Dev 12:2164-2174.
54. Sheng M, Dougan ST, McFadden G, Greenberg ME (1988) Calcium and growth factor pathways of c-fos transcriptional activation require distinct upstream regulatory sequences. Mol Cell Biol 8:2787-2796.
55. Spencer JA, Misra RP (1996) Expression of the serum response factor gene is regulated by serum response factor binding sites. J Biol Chem 271:16535-16543.
56. Troy CM, Rabacchi SA, Hohl JB, Angelastro JM, Greene LA, Shelanski ML (2001) Death in the balance: Alternative participation of the caspase-2 and -9 pathways in neuronal death induced by nerve growth factor deprivation. J Neurosci 21:5007-5016.
57. Tsuji M, Inanami O, Kuwabara M (2001) Induction of neurite outgrowth in PC12 cells by alpha-phenyl-N-tert-butylnitron through activation of protein kinase C and the Ras-extracellular signal-regulated kinase pathway. J Biol Chem 276:32779-32785.
58. Uberall F, Giselbrecht S, Hellbert K, Fresser F, Bauer B, Gschwendt M, Grunicke HH, Baier G (1997) Conventional PKC-alpha, novel PKC-epsilon and PKC-theta, but not atypical PKC-lambda are MARCKS kinases in intact NIH 3T3 fibroblasts. J Biol Chem 272:4072-4078.
59. Uberall F, Hellbert K, Kampfer S, Maly K, Villunger A, Spitaler M, Mwanjewe J, Baier-Bitterlich G, Baier G, Grunicke HH (1999) Evidence that atypical protein kinase C-lambda and atypical protein kinase C-zeta participate in Ras-mediated reorganization of the F-actin cytoskeleton. J Cell Biol 144:413-425.
60. Varnum BC, Ma QF, Chi TH, Fletcher B, Herschman HR (1991) The TIS11 primary response gene is a member of a gene family that encodes proteins with a highly conserved sequence containing an unusual Cys-His repeat. Mol Cell Biol 11:1754-1758.
61. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484-487.
62. Velculescu VE, Vogelstein B, Kinzler KW (2000) Analysing uncharted transcriptomes with SAGE. Trends Genet 16:423-425.
63. Vlahos CJ, Matter WF, Hui KY, Brown RF (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.
64. Wooten MW, Zhou G, Seibenhener ML, Coleman ES (1994) A role for zeta protein kinase C in nerve growth factor-induced differentiation of PC12 cells. Cell Growth Differ 5:395-403.
65. Wooten MW, Zhou G, Wooten MC, Seibenhener ML (1997) Transport of protein kinase C isoforms to the nucleus of PC12 cells by nerve growth factor: Association of atypical zeta-PKC with the nuclear matrix. J Neurosci Res 49:393-403.
66. Wooten MW, Seibenhener ML, Zhou G, Vandenplas ML, Tan TH (1999) Overexpression of atypical PKC in PC12 cells enhances NGF-responsiveness and survival through an NF-kappaB dependent pathway. Cell Death Differ 6:753-764.
67. Wooten MW, Seibenhener ML, Neidigh KB, Vandenplas ML (2000) Mapping of atypical protein kinase C within the nerve growth factor signaling cascade: Relationship to differentiation and survival of PC12 cells. Mol Cell Biol 20:4494-4504.
68. Wooten MW, Seibenhener ML, Mamidipudi V, Diaz-Meco MT, Barker PA, Moscat J (2001) The atypical protein kinase C-interacting protein p62 is a scaffold for NF-kappaB activation by nerve growth factor. J Biol Chem 276:7709-7712.
69. Wu BY, Fodor EJ, Edwards RH, Rutter WJ (1989) Nerve growth factor induces the proto-oncogene c-jun in PC12 cells. J Biol Chem 264:9000-9003.
70. Yamamoto M, Wakatsuki T, Hada A, Ryo A (2001) Use of serial analysis of gene expression (SAGE) technology. J Immunol Methods 250:45-66.
71. Yoh K, Sugawara T, Motohashi H, Takahama Y, Koyama A, Yamamoto M, Takahashi S (2001) Transgenic over-expression of MafK suppresses T cell proliferation and function in vivo. Genes Cells 6:1055-1066.
72. Zheng WH, Kar S, Quirion R (2000) Stimulation of protein kinase C modulates insulin-like growth factor-1-induced akt activation in PC12 cells. J Biol Chem 275:13377-13785.