Nerve growth factor induces transcription of the p21 WAF1/CIP1 and cyclin D1 genes in PC12 cells by activating the Sp1 transcription factor

Journal of Neuroscience

Volumn 17, Issue 16, 1997, Pages 6122-6132

  Yan, Guo Zai ^a   Ziff, Edward B ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cell cycle; Cyclin D1; NGF; p21 WAF1 CIP1 Sdi1; PC12; Sp1

Indexed keywords

CYCLINE; NERVE GROWTH FACTOR; PROTEIN P21; TRANSCRIPTION FACTOR SP1;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL CYCLE; GENE ACTIVATION; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION INITIATION;

EID: 0030758522     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-16-06122.1997     Document Type: Article

References (100)

1. Akagi M, Yasui W, Akama Y, Yokozaki H, Tahara H, Haruma K, Kajiyama G, Tahara E (1996) Inhibition of cell growth by transforming growth factor beta 1 is associated with p53-independent induction of p21 in gastric carcinoma cells. Jpn J Cancer Res 87:377-384.
2. Aloe L, Levi MR (1979) Nerve growth factor-induced transformation of immature chromaffin cells in vivo into sympathetic neurons: effect of antiserum to nerve growth factor. Proc Natl Acad Sci USA 76:1246-1250.
3. Anderson DJ, Axel R (1986) A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. Cell 47:1079-1090.
4. Baldin V, Lukas J, Marcote MJ, Pagano M, Draetta G (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev 7:812-821.
5. Bates S, Bonetta L, MacAllan D, Parry D, Holder A, Dickson C, Peters G (1994) CDK6 (PLSTIRE) and CDK4 (PSK-J3) are a distinct subset of the cyclin-dependent kinases that associate with cyclin D1. Oncogene 9:71-79.
6. Beijersbergen RL, Bernards R (1996) Cell cycle regulation by the retinoblastoma family of growth inhibitory proteins [review]. Biochim Biophys Acta 1287:103-120.
7. Biggs JR, Kudlow JE, Kraft AS (1996) The role of the transcription factor Sp1 in regulating the expression of the WAF1/CIP1 gene in U937 leukemic cells. J Biol Chem 271:901-906.
8. Billon N, van Grunsven LA, Rudkin BB (1996) The CDK inhibitor p21WAF1/Cip1 is induced through a p300-dependent mechanism during NGF-mediated neuronal differentiation of PC12 cells. Oncogene 13:2047-2054.
9. Boonstra J, Moolenaar WH, Harrison PH, Moed P, van der Saag PT, de Laat SW (1983) Ionic responses and growth stimulation induced by nerve growth factor and epidermal growth factor in rat pheochromocytoma (PC12) cells. J Cell Biol 97:92-98.
10. Boulton TG, Nye SH, Robbins DJ, Ip NY, Radziejewska E, Morgenbesser SD, DePinho RA, Panayotatos N, Cobb MH, Yancopoulos GD (1991) ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65:663-675.
11. Boulukos KE, Ziff EB (1993) Adenovirus 5 E1A proteins disrupt the neuronal phenotype and growth factor responsiveness of PC12 cells by a conserved region 1-dependent mechanism. Oncogene 8:237-248.
12. Buchkovich KJ, Ziff EB (1994) Nerve growth factor regulates the expression and activity of p33cdk2 and p34cdc2 kinases in PC12 pheochromocytoma cells. Mol Biol Cell 5:1225-1241.
13. Burstein DE, Greene LA (1982) Nerve growth factor has both mitogenic and antimitogenic activity. Dev Biol 94:477-482.
14. Cathala G, Savoucet J-F, Mendez B, West BL, Karin M, Martial JA, Baxter JD (1983) A method for isolation of intact translationally active ribonucleic acid. DNA 2:329-335.
15. Chen J, Jackson PK, Kirschner MW, Dutta A (1995a) Separate domains of p21 involved in the inhibition of Cdk kinase and PCNA. Nature 374:386-388.
16. Chen PL, Riley DJ, Lee WH (1995b) The retinoblastoma protein as a fundamental mediator of growth and differentiation signals [review]. Crit Rev Eukaryot Gene Expr 5:79-95.
17. Chiang CM, Roeder RG (1995) Cloning of an intrinsic human TFIID subunit that interacts with multiple transcriptional activators. Science 267:531-536.
18. Chin LS, Li L, Greengard P (1994) Neuron-specific expression of the synapsin II gene is directed by a specific core promoter and upstream regulatory elements. J Biol Chem 269:18507-18513.
19. Cibelli G, Schoch S, Pajunk H, Brand IA, Thiel G (1996) A (G+C)-rich motif in the aldolase C promoter functions as a constitutive transcriptional enhancer element. Eur J Biochem 237:311-317.
20. Courey AJ, Tjian R (1988) Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell 55:887-898.
21. Courey AJ, Holtzman DA, Jackson SP, Tjian R (1989) Synergistic activation by the glutamine-rich domains of human transcription factor Sp1. Cell 59:827-836.
22. Cowley S, Paterson H, Kemp P, Marshall CJ (1994) Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77:841-852.
23. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF (1995a) Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci USA 92:5545-5549.
24. Datto MB, Yu Y, Wang XF (1995b) Functional analysis of the transforming growth factor beta responsive elements in the WAF1/Cip1/p21 promoter. J Biol Chem 270:28623-28628.
25. Dignam JD, Lebowitz RM, Roeder RG (1983) Accurate transcription initiation by RNA polymerase II is a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 14:1475-1489.
26. Dobashi Y, Kudoh T, Matsumine A, Toyoshima K, Akiyama T (1995) Constitutive overexpression of CDK2 inhibits neuronal differentiation of rat pheochromocytoma PC12 cells. J Biol Chem 270:23031-23037.
27. 1 cyclins in senescent human diploid fibroblasts: accumulation of inactive cyclin E-Cdk2 and cyclin D1-Cdk2 complexes. Proc Natl Acad Sci USA 90:11034-11038.
28. 1 arrest. Cell 76:1013-1023.
29. Eizenberg O, Faber EA, Gottlieb E, Oren M, Rotter V, Schwartz M (1996) p53 plays a regulatory role in differentiation and apoptosis of central nervous system-associated cells. Mol Cell Biol 16:5178-5185.
30. El-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B (1993) WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
31. Elder GA, Liang Z, Lee N, Friedrich VJ, Lazzarini RA (1992) Novel DNA binding proteins participate in the regulation of human neurofilament H gene expression. Brain Res Mol Brain Res 15:85-98.
32. Faraonio R, Minopoli G, Porcellini A, Costanzo F, Cimino F, Russo T (1994) The DNA sequence encompassing the transcription start site of a TATA-less promoter contains enough information to drive neuron-specific transcription. Nucleic Acids Res 22:4876-4883.
33. Freeman RS, Estus S, Johnson EJ (1994) Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of Cyclin D1 during programmed cell death. Neuron 12:343-355.
34. Gao CY, Zelenka PS (1997) Cyclins, cyclin-dependent kinases and differentiation. BioEssays 19:307-315.
35. Gill G, Pascal E, Tseng ZH, Tjian R (1994) A glutamine-rich hydrophobic patch in transcription factor Sp1 contacts the dTAFII110 component of the Drosophila TFIID complex and mediates transcriptional activation. Proc Natl Acad Sci USA 91:192-196.
36. Gizang GE, Ziff EB (1990) Nerve growth factor regulates tyrosine hydroxylase gene transcription through a nucleoprotein complex that contains c-Fos. Genes Dev 4:477-491.
37. Gomez N, Cohen P (1991) Dissection of the protein kinase cascade by which nerve growth factor activates MAP kinases. Nature 353:170-173.
38. Gomez N, Tonks NK, Morrison C, Harmar T, Cohen P (1990) Evidence for communication between nerve growth factor and protein tyrosine phosphorylation. FEBS Lett 271:119-122.
39. Gotoh Y, Nishida E, Yamashita T, Hoshi M, Kawakami M, Sakai H (1990) Microtubule-associated-protein (MAP) kinase activated by nerve growth factor and epidermal growth factor in PC12 cells: identity with the mitogen-activated MAP kinase of fibroblastic cells. Eur J Biochem 193:661-669.
40. Greenberg ME, Hermanowski AL, Ziff EB (1986) Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription. Mol Cell Biol 6:1050-1057.
41. Greene LA (1978) Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium. J Cell Biol 78:747-755.
42. 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.
43. Gunning PW, Landreth GE, Layer P, Ignatius M, Shooter EM (1981) Nerve growth factor-induced differentiation of PC12 cells: evaluation of changes in RNA and DNA metabolism. J Neurosci 1:368-379.
44. Hagen G, Dennig J, Preiss A, Beato M, Suske G (1995) Functional analyses of the transcription factor Sp4 reveal properties distinct from Sp1 and Sp3. J Biol Chem 270:24989-24994.
45. Hahn M, Hahn SL, Stone DM, Joh TH (1992) Cloning of the rat gene encoding choline acetyltransferase, a cholinergic neuron-specific marker. Proc Natl Acad Sci USA 89:4387-4391.
46. Harper JW, Elledge SJ, Keyomarsi K, Dynlacht B, Tsai L H, Zhang P, Dobrowolski S, Bai C, Connell CL, Swindell E, Fox MP, Wei N (1995) Inhibition of cyclin-dependent kinases by p21. Mol Biol Cell 6:387-400.
47. Hoey T, Weinzierl RO, Gill G, Chen JL, Dynlacht BD, Tjian R (1993) Molecular cloning and functional analysis of Drosophila TAF110 reveal properties expected of coactivators. Cell 72:247-260.
48. Ignatius MJ, Chandler CR, Shooter EM (1985) Nerve growth factor-treated, neurite-bearing PC12 cells continue to synthesize DNA. J Neurosci 5:343-351.
49. Jackson SP, MacDonald JJ, Lees MS, Tjian R (1990) GC box binding induces phosphorylation of Sp1 by a DNA-dependent protein kinase. Cell 63:155-165.
50. Jiang H, Lin J, Su ZZ, Collart FR, Huberman E, Fisher PB (1994) Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene 9:3397-3406.
51. Jiang W, Kahn SM, Tomita N, Zhang YJ, Lu SH, Weinstein IB (1992) Amplification and expression of the human cyclin D gene in esophageal cancer. Cancer Res 52:2980-2983.
52. Jiang W, Kahn SM, Zhou P, Zhang YJ, Cacace AM, Infante AS, Doi S, Santella RM, Weinstein IB (1993) Overexpression of cyclin D1 in rat fibroblasts causes abnormalities in growth control, cell cycle progression and gene expression. Oncogene 8:3447-3457.
53. Juan G, Gong J, Traganos F, Darzynkiewicz Z (1996) Unscheduled expression of cyclins D1 and D3 in human tumour cell lines. Cell Proliferation 29:259-266.
54. Kadonaga JT, Carner KR, Masiarz FR, Tjian R (1987) Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain. Cell 51:1079-1090.
55. Kallunki P, Jenkinson S, Edelman GM, Jones FS (1995) Silencer elements modulate the expression of the gene for the neuron-glia cell adhesion molecule, Ng-CAM. J Biol Chem 270:21291-21298.
56. Kiess M, Gill RM, Hamel PA (1995) Expression of the positive regulator of cell cycle progression, cyclin D3, is induced during differentiation of myoblasts into quiescent myotubes. Oncogene 10:159-166.
57. Kim SJ, Onwuta US, Lee YI, Li R, Botchan MR, Robbins PD (1992) The retinoblastoma gene product regulates Sp1-mediated transcription. Mol Cell Biol 12:2455-2463.
58. Kingsley C, Winoto A (1992) Cloning of GT box-binding proteins: a novel Sp1 multigene family regulating T-cell receptor gene expression. Mol Cell Biol 12:4251-4261.
59. Kranenburg O, van der Eb AJ, Zantema A (1996) Cyclin D1 is an essential mediator of apoptotic neuronal cell death. EMBO J 15:46-54.
60. MAPK pathway. J Biol Chem 271:20608-20616.
61. Leonard DG, Ziff EB, Green LA (1987) Identification and characterization of mRNAs regulated by nerve growth factor in PC12 cells. Mol Cell Biol 7:3156-3167.
62. Leonard DG, Gorham JD, Cole P, Greene LA, Ziff EB (1988) A nerve growth factor-regulated messenger RNA encodes a new intermediate filament protein. J Cell Biol 106:181-193.
63. Li JM, Nichols MA, Chandrasekharan S, Xiong Y, Wang XF (1995) Transforming growth factor beta activates the promoter of cyclin-dependent kinase inhibitor p15INK4B through an Sp1 consensus site. J Biol Chem 270:26750-26753.
64. Li LH, Nerlov C, Prendergast G, MacGregor D, Ziff EB (1994) c-Myc represses transcription in vivo by a novel mechanism dependent on the initiator element and Myc box II. EMBO J 13:4070-4079.
65. Li R, Waga S, Hannon GJ, Beach D, Stillman B (1994) Differential effects by the p21 CDK inhibitor on PCNA-dependent DNA replication and repair. Nature 371:534-537.
66. Li R, Hannon GJ, Beach D, Stillman B (1996) Subcellular distribution of p21 and PCNA in normal and repair-deficient cells following DNA damage. Curr Biol 6:189-199.
67. Liu M, Lee MH, Cohen M, Bommakanti M, Freedman LP (1996) Transcriptional activation of the Cdk inhibitor p21 by vitamin D3 leads to the induced differentiation of the myelomonocytic cell line U937. Genes Dev 10:142-153.
68. Liu Y, Martindale JL, Gorospe M, Holbrook NJ (1996) Regulation of p21WAF1/CIP1 expression through mitogen-activated protein kinase signaling pathway. Cancer Res 56:31-35.
69. Luo Y, Hurwitz J, Massague J (1995) Cell-cycle inhibition by independent CDK and PCNA binding domains in p21Cip1. Nature 375:159-161.
70. Macleod KF, Sherry N, Hannon G, Beach D, Tokino T, Kinzler K, Vogelstein B, Jacks T (1995) p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev 9:935-944.
71. Matsushime H, Roussel MF, Ashmun RA, Sherr CJ (1991) Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 65:701-713.
72. Matsushime H, Ewen ME, Strom DK, Kato JY, Hanks SK, Roussel MF, Sherr CJ (1992) Identification and properties of an atypical catalytic subunit (p34PSK-J3/cdk4) for mammalian D type G1 cyclins. Cell 71:323-334.
73. Pagano M, Theodoras AM, Tam SW, Draetta GF (1994) Cyclin D1-mediated inhibition of repair and replicative DNA synthesis in human fibroblasts. Genes Dev 8:1627-1639.
74. Parker SB, Eichele G, Zhang P, Rawls A, Sands AT, Bradley A, Olson EN, Harper JW, Elledge SJ (1995) p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science 267:1024-1027.
75. Peter M, Herskowitz I (1994) Joining the complex: cyclin-dependent kinase inhibitory proteins and the cell cycle. Cell 79:181-184.
76. Poluha W, Poluha DK, Chang B, Crosbie NE, Schonhoff CM, Kilpatrick DL, Ross AH (1996) The cyclin-dependent kinase inhibitor p21 (WAF1) is required for survival of differentiating neuroblastoma cells. Mol Cell Biol 16:1335-1341.
77. Prowse DM, Bolgan L, Molnar A, Dotto GP (1997) Involvement of the Sp3 transcription factor in induction of p21Cip1/WAF1 in keratinocyte differentiation. J Biol Chem 272:1308-1314.
78. Rao SS, Kohtz DS (1995) Positive and negative regulation of D-type cyclin expression in skeletal myoblasts by basic fibroblast growth factor and transforming growth factor beta: a role for cyclin D1 in control of myoblast differentiation. J Biol Chem 270:4093-4100.
79. Reeben M, Myohanen S, Saarma M, Prydz H (1995) Sequencing of the rat light neurofilament promoter reveals differences in methylation between expressing and non-expressing cell lines, but not tissues. Gene 157:325-329.
80. Ross ME, Carter ML, Lee JH (1996) MN20, a D2 cyclin, is transiently expressed in selected neural populations during embryogenesis. J Neurosci 16:210-219.
81. Rudkin BB, Lazarovici P, Levi BZ, Abe Y, Fujita K, Guroff G (1989) Cell cycle-specific action of nerve growth factor in PC12 cells: differentiation without proliferation. EMBO J 8:3319-3325.
82. Ryabinin AE, Sato TN, Morris PJ, Latchman DS, Wilson MC (1995) Immediate upstream promoter regions required for neurospecific expression of SNAP-25. J Mol Neurosci 6:201-210.
83. Shambaugh III GE, Lee RJ, Watanabe G, Erfurth F, Karnezis AN, Koch AE, Haines III GK, Halloran M, Brody BA, Pestell RG (1996) Reduced cyclin D1 expression in the cerebella of nutritionally deprived rats correlates with developmental delay and decreased cellular DNA synthesis. J Neuropathol Exp Neurol 55:1009-1020.
84. Sherr CJ (1995) D-type cyclins. Trends Biochem Sci 20:187-190.
85. Sicinski P, Donaher JL, Parker SB, Li T, Fazeli A, Gardner H, Haslam SZ, Bronson RT, Elledge SJ, Weinberg RA (1995) Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82:621-630.
86. Sif S, Gilmore TD (1994) Interaction of the v-Raf oncoprotein with cellular transcription factor Sp1. J Virol 68:7131-7138.
87. Soto AM, Sonnenschein C (1985) The role of estrogens on the proliferation of human breast tumor cells (MCF-7). J Steroid Biochem 23:87-94.
88. Steinman RA, Hoffman B, Iro A, Guillouf C, Liebermann DA, el-Houseini ME (1994) Induction of p21 (WAF-1/CIP1) during differentiation. Oncogene 9:3389-3396.
89. Tamaru T, Trigun SK, Okada M, Nakagawa H (1993) Identification of cells expressing a D type G1 cyclin in matured brain: implication for its role in neuronal function. Neurosci Lett 153:169-172.
90. Traverse S, Gomez N, Paterson H, Marshall C, Cohen P (1992) Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells: comparison of the effects of nerve growth factor and epidermal growth factor. Biochem J 288:351-355
91. Udvadia AJ, Templeton DJ, Horowitz JM (1995) Functional interactions between the retinoblastoma (Rb) protein and Sp-family members: superactivation by Rb requires amino acids necessary for growth suppression. Proc Natl Acad Sci USA 92:3953-3957.
92. Unsicker K, Krisch B, Otten U, Thoenen H (1978) Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids. Proc Natl Acad Sci USA 75:3498-3502.
93. van Grunsven LA, Thomas A, Urdiales JL, Machenaud S, Choler P, Durand I, Rudkin BB (1996a) Nerve growth factor-induced accumulation of PC12 cells expressing cyclin D1: evidence for a G1 phase block. Oncogene 12:855-862.
94. van Grunsven LA, Billon N, Savatier P, Thomas A, Urdiales JL, Rudkin BB (1996b) Effect of nerve growth factor on the expression of cell cycle regulatory proteins in PC12 cells: dissection of the neurotrophic response from the anti-mitogenic response. Oncogene 12:1347-1356.
95. Vlach J, Garcia A, Jacque JM, Rodriguez MS, Michelson S, Virelizier JL (1995) Induction of Sp1 phosphorylation and NF-kappa B-independent HIV promoter domain activity in T lymphocytes stimulated by okadaic acid. Virology 208:753-761.
96. Waga S, Hannon GJ, Beach D, Stillman B (1994) The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369:574-578.
97. Wang OS, Sabourin CL, Wang H, Stoner GD (1996) Overexpression of cyclin D1 and cyclin E in N-nitrosomethylbenzylamine-induced rat esophageal tumorigenesis. Carcinogenesis 17:1583-1588.
98. Van GZ, Ziff EB (1995) NGF regulates the PC12 cell cycle machinery through specific inhibition of the Cdk kinases and induction of cyclin D1. J Neurosci 15:6200-6212.
99. Zeng YX, Somasundaram K, el-Deiry WS (1997) AP2 inhibits cancer cell growth and activates p21WAF1/CIP1 expression. Nat Genet 15:78-82.
100. Zhang H, Hannon GJ, Beach D (1994) p21-containing cyclin kinases exist in both active and inactive states. Genes Dev 8:1750-1758.