NGF-Induced Cell Differentiation and Gene Activation Is Mediated by Integrative Nuclear FGFR1 Signaling (INFS)

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Lee, Yu Wei ^a   Stachowiak, Ewa K ^a,b   Birkaya, Barbara ^a   Terranova, Christopher ^a,b   Capacchietti, Mariolina ^a   Claus, Peter ^d,e   Aletta, John M ^c   Stachowiak, Michal K ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b Western New York Stem Cells Culture and Analysis Center   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLECORTIN; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; NERVE GROWTH FACTOR; NUCLEAR RECEPTOR NUR77; NUCLEAR RECEPTOR RELATED FACTOR 1; TYROSINE 3 MONOOXYGENASE;

ARTICLE; BETAIII TUBULIN GENE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DCX GENE; FGF 2 GENE; FGFR1 GENE; GENE ACTIVATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NUR77 GENE; NURR1 GENE; PC12 CELL; PROMOTER REGION; PROTEIN MOTIF; PROTEIN TRANSPORT; TH GENE; TYROSINE HYDROXYLASE GENE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL DIFFERENTIATION; CELL NUCLEUS; CELLS, CULTURED; HUMANS; NERVE GROWTH FACTOR; NEURITES; PC12 CELLS; PROTEIN TRANSPORT; RATS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84879996732     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068931     Document Type: Article

References (73)

1. Stachowiak EK, Fang X, Myers J, Dunham S, Stachowiak MK, (2003) cAMP-induced differentiation of human neuronal progenitor cells is mediated by nuclear fibroblast growth factor receptor-1 (FGFR1). J Neurochem 84: 1296-1312.
2. Stachowiak MK, Maher PA, Joy A, Mordechai E, Stachowiak EK, (1996) Nuclear accumulation of fibroblast growth factor receptors is regulated by multiple signals in adrenal medullary cells. Mol Biol Cell 7: 1299-1317.
3. Levi-Montalcini R, (1987) The nerve growth factor 35 years later. Science 237: 1154-1162.
4. Scimeca JC, Nguyen TT, Filloux C, Van Obberghen E, (1992) Nerve growth factor-induced phosphorylation cascade in PC12 pheochromocytoma cells. Association of S6 kinase II with the microtubule-associated protein kinase, ERK1. J Biol Chem 267: 17369-17374.
5. Sofroniew MV, Howe CL, Mobley WC, (2001) Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 24: 1217-1281.
6. 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 U S A 73: 2424-2428.
7. Greene LA, (1984) The importance of both early and delayed responses in the biological actions of nerve growth factor. Trends in Neurosciences 7: 91-94.
8. Greene LA, Tischler AS (1982) PC12 pheochromocytomacultures in neurobiologicalresearch. Adv Cell Neurobiol.
9. Neufeld G, Gospodarowicz D, Dodge L, Fujii DK, (1987) Heparin modulation of the neurotropic effects of acidic and basic fibroblast growth factors and nerve growth factor on PC12 cells. J Cell Physiol 131: 131-140.
10. Szeberenyi J, Erhardt P, (1994) Cellular components of nerve growth factor signaling. Biochim Biophys Acta 1222: 187-202.
11. Xing J, Kornhauser JM, Xia Z, Thiele EA, Greenberg ME, (1998) Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol Cell Biol 18: 1946-1955.
12. Milbrandt J, (1988) Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron 1: 183-188.
13. Silverman E, Frodin M, Gammeltoft S, Maller JL, (2004) Activation of p90 Rsk1 is sufficient for differentiation of PC12 cells. Mol Cell Biol 24: 10573-10583.
14. 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.
15. Backman C, Perlmann T, Wallen A, Hoffer BJ, Morales M, (1999) A selective group of dopaminergic neurons express Nurr1 in the adult mouse brain. Brain Res 851: 125-132.
16. Woronicz JD, Calnan B, Ngo V, Winoto A, (1994) Requirement for the orphan steroid receptor Nur77 in apoptosis of T-cell hybridomas. Nature 367: 277-281.
17. Zetterstrom RH, Solomin L, Jansson L, Hoffer BJ, Olson L, et al. (1997) Dopamine neuron agenesis in Nurr1-deficient mice. Science 276: 248-250.
18. Castillo SO, Baffi JS, Palkovits M, Goldstein DS, Kopin IJ, et al. (1998) Dopamine biosynthesis is selectively abolished in substantia nigra/ventral tegmental area but not in hypothalamic neurons in mice with targeted disruption of the Nurr1 gene. Mol Cell Neurosci 11: 36-46.
19. Saucedo-Cardenas O, Quintana-Hau JD, Le WD, Smidt MP, Cox JJ, et al. (1998) Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc Natl Acad Sci U S A 95: 4013-4018.
20. Kolluri SK, Bruey-Sedano N, Cao X, Lin B, Lin F, et al. (2003) Mitogenic effect of orphan receptor TR3 and its regulation by MEKK1 in lung cancer cells. Mol Cell Biol 23: 8651-8667.
21. Maruoka H, Sasaya H, Shimamura Y, Nakatani Y, Shimoke K, et al. (2010) Dibutyryl-cAMP up-regulates nur77 expression via histone modification during neurite outgrowth in PC12 cells. J Biochem 148: 93-101.
22. Hu Y, Fang X, Dunham SM, Prada C, Stachowiak EK, et al. (2004) 90-kDa ribosomal S6 kinase is a direct target for the nuclear fibroblast growth factor receptor 1 (FGFR1): role in FGFR1 signaling. J Biol Chem 279: 29325-29335.
23. Fang X, Stachowiak EK, Dunham-Ems SM, Klejbor I, Stachowiak MK, (2005) Control of CREB-binding protein signaling by nuclear fibroblast growth factor receptor-1: a novel mechanism of gene regulation. J Biol Chem 280: 28451-28462.
24. Lee YW, Terranova C, Birkaya B, Narla S, Kehoe D, et al. (2012) A novel nuclear FGF Receptor-1 partnership with retinoid and Nur receptors during developmental gene programming of embryonic stem cells. J Cell Biochem 113: 2920-2936.
25. Baron O, Forthmann B, Lee YW, Terranova C, Ratzka A, et al. (2012) Cooperation of nuclear fibroblast growth factor receptor 1 and nurr1 offers new interactive mechanism in postmitotic development of mesencephalic dopaminergic neurons. J Biol Chem 287: 19827-19840.
26. Peng H, Moffett J, Myers J, Fang X, Stachowiak EK, et al. (2001) Novel nuclear signaling pathway mediates activation of fibroblast growth factor-2 gene by type 1 and type 2 angiotensin II receptors. Mol Biol Cell 12: 449-462.
27. Stachowiak MK, Fang X, Myers JM, Dunham SM, Berezney R, et al. (2003) Integrative nuclear FGFR1 signaling (INFS) as a part of a universal "feed-forward-and-gate" signaling module that controls cell growth and differentiation. J Cell Biochem 90: 662-691.
28. Stachowiak MK, Maher PA, Stachowiak EK, (2007) Integrative Nuclear Signaling in Cell Development-A Role for FGF Receptor-1. DNA Cell Biol 26: 811-826.
29. Stachowiak EK, Roy I, Lee Y-W, Capacchietti M, Aletta JM, et al. (2009) Targeting novel Integrative Nuclear FGFR1 Signaling by nanoparticle-mediated gene transfer stimulates neurogenesis in adult brain. Integrative Biology 1: 394-403.
30. Stachowiak MK, Stachowiak EK, Aletta JM, Tzanakakis ES (2011) A common integrative nuclear signaling module for stem cell development. In: M.K. Stachowiak EST, editor. Stem Cells from mechanisms to technologies: World Scientific.
31. Myers JM, Martins GG, Ostrowski J, Stachowiak MK, (2003) Nuclear trafficking of FGFR1: a role for the transmembrane domain. J Cell Biochem 88: 1273-1291.
32. Dunham-Ems SM, Lee YW, Stachowiak EK, Pudavar H, Claus P, et al. (2009) Fibroblast growth factor receptor-1 (FGFR1) nuclear dynamics reveal a novel mechanism in transcription control. Mol Biol Cell 20: 2401-2412.
33. Dunham-Ems SM, Pudavar HE, Myers JM, Maher PA, Prasad PN, et al. (2006) Factors controlling fibroblast growth factor receptor-1's cytoplasmic trafficking and its regulation as revealed by FRAP analysis. Mol Biol Cell 17: 2223-2235.
34. Reilly JF, Maher PA, (2001) Importin beta-mediated nuclear import of fibroblast growth factor receptor: role in cell proliferation. J Cell Biol 152: 1307-1312.
35. Dunham-Ems SM, Lee YW, Stachowiak EK, Pudavar H, Claus P,et al. (2009) Fibroblast Growth Factor Receptor-1 (FGFR1) Nuclear Dynamics Reveal a Novel Mechanism in Transcription Control. Mol Biol Cell.
36. Peng H, Myers J, Fang X, Stachowiak EK, Maher PA, et al. (2002) Integrative nuclear FGFR1 signaling (INFS) pathway mediates activation of the tyrosine hydroxylase gene by angiotensin II, depolarization and protein kinase C. J Neurochem. 81: 506-524.
37. Kim EL, Esparza FM, Stachowiak MK, (1996) The roles of CRE, TRE, and TRE-adjacent S1 nuclease sensitive element in the regulation of tyrosine hydroxylase gene promoter activity by angiotensin II. J Neurochem 67: 26-36.
38. Niwa H, Yamamura K, Miyazaki J, (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199.
39. Maira M, Martens C, Philips A, Drouin J, (1999) Heterodimerization between members of the Nur subfamily of orphan nuclear receptors as a novel mechanism for gene activation. Mol Cell Biol 19: 7549-7557.
40. Maira M, Martens C, Batsche E, Gauthier Y, Drouin J, (2003) Dimer-specific potentiation of NGFI-B (Nur77) transcriptional activity by the protein kinase A pathway and AF-1-dependent coactivator recruitment. Mol Cell Biol 23: 763-776.
41. Hanneken A, Maher PA, Baird A, (1995) High affinity immunoreactive FGF receptors in the extracellular matrix of vascular endothelial cells-implications for the modulation of FGF-2. J Cell Biol 128: 1221-1228.
42. Somanathan S, Stachowiak EK, Siegel AJ, Stachowiak MK, Berezney R, (2003) Nuclear matrix bound fibroblast growth factor receptor is associated with splicing factor rich and transcriptionally active nuclear speckles. J Cell Biochem 90: 856-869.
43. Chioni AM, Grose R, (2012) FGFR1 cleavage and nuclear translocation regulates breast cancer cell behavior. J Cell Biol 197: 801-817.
44. 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.
45. Sen N, Hara MR, Kornberg MD, Cascio MB, Bae BI, et al. (2008) Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat Cell Biol 10: 866-873.
46. Kornberg MD, Sen N, Hara MR, Juluri KR, Nguyen JV, et al. (2010) GAPDH mediates nitrosylation of nuclear proteins. Nat Cell Biol 12: 1094-1100.
47. Stachowiak EK, Maher PA, Tucholski J, Mordechai E, Joy A, et al. (1997) Nuclear accumulation of fibroblast growth factor receptors in human glial cells-association with cell proliferation. Oncogene 14: 2201-2211.
48. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
49. Stachowiak MK, Moffett J, Maher P, Tucholski J, Stachowiak EK, (1997) Growth factor regulation of cell growth and proliferation in the nervous system. A new intracrine nuclear mechanism. Mol Neurobiol 15: 257-283.
50. Kudo N, Wolff B, Sekimoto T, Schreiner EP, Yoneda Y, et al. (1998) Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp Cell Res 242: 540-547.
51. Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner EP, et al. (1999) Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci U S A 96: 9112-9117.
52. Joshi HC, Cleveland DW, (1989) Differential utilization of beta-tubulin isotypes in differentiating neurites. J Cell Biol 109: 663-673.
53. Fischer I, Richter-Landsberg C, Safaei R, (1991) Regulation of microtubule associated protein 2 (MAP2) expression by nerve growth factor in PC12 cells. Exp Cell Res 194: 195-201.
54. Lee V, Trojanowski JQ, Schlaepfer WW, (1982) Induction of neurofilament triplet proteins in PC12 cells by nerve growth factor. Brain Res 238: 169-180.
55. Lindenbaum MH, Carbonetto S, Mushynski WE, (1987) Nerve growth factor enhances the synthesis, phosphorylation, and metabolic stability of neurofilament proteins in PC12 cells. J Biol Chem 262: 605-610.
56. Casado M, Lopez-Guajardo A, Mellstrom B, Naranjo JR, Lerma J, (1996) Functional N-methyl-D-aspartate receptors in clonal rat phaeochromocytoma cells. J Physiol 490 (Pt 2): 391-404.
57. Rogers SW, Mandelzys A, Deneris ES, Cooper E, Heinemann S, (1992) The expression of nicotinic acetylcholine receptors by PC12 cells treated with NGF. J Neurosci 12: 4611-4623.
58. Nikodijevic B, Guroff G, (1991) Nerve growth factor-induced increase in calcium uptake by PC12 cells. Journal of Neuroscience Research 28: 192-199.
59. O'Lague PH, Huttner SL, Vandenberg CA, Morrison-Graham K, Horn R, (1985) Morphological properties and membrane channels of the growth cones induced in PC12 cells by nerve growth factor. J Neurosci Res 13: 301-321.
60. Ghee M, Baker H, Miller JC, Ziff EB, (1998) AP-1, CREB and CBP transcription factors differentially regulate the tyrosine hydroxylase gene. Brain Res Mol Brain Res 55: 101-114.
61. Angelastro JM, Klimaschewski L, Tang S, Vitolo OV, Weissman TA, et al. (2000) Identification of diverse nerve growth factor-regulated genes by serial analysis of gene expression (SAGE) profiling. Proc Natl Acad Sci U S A 97: 10424-10429.
62. Nacher J, Crespo C, McEwen BS, (2001) Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14: 629-644.
63. Bharali DJ, Klejbor I, Stachowiak EK, Dutta P, Roy I, et al. (2005) Organically modified silica nanoparticles: a nonviral vector for in vivo gene delivery and expression in the brain. Proc Natl Acad Sci U S A 102: 11539-11544.
64. Stachowiak EK, Roy I, Stachowiak,MK (2011) Triggering neuronogenesis by endogenous brain stem cells with DNA nanoplexes. In: M.K. Stachowiak EST, editor. Stem Cells from Mechanisms to Technologies: World Scientific Publishing.
65. Chevet E, Lemaitre G, Janjic N, Barritault D, Bikfalvi A, et al. (1999) Fibroblast growth factor receptors participate in the control of mitogen-activated protein kinase activity during nerve growth factor-induced neuronal differentiation of PC12 cells. J Biol Chem 274: 20901-20908.
66. Meisinger C, Hertenstein A, Grothe C, (1996) Fibroblast growth factor receptor 1 in the adrenal gland and PC12 cells: developmental expression and regulation by extrinsic molecules. Brain Res Mol Brain Res 36: 70-78.
67. Hirata Y, Whalin M, Ginty DD, Xing J, Greenberg ME, et al. (1995) Induction of a nerve growth factor-sensitive kinase that phosphorylates the DNA-binding domain of the orphan nuclear receptor NGFI-B. J Neurochem 65: 1780-1788.
68. Kang SA, Na H, Kang HJ, Kim SH, Lee MH, et al. (2010) Regulation of Nur77 protein turnover through acetylation and deacetylation induced by p300 and HDAC1. Biochem Pharmacol 80: 867-873.
69. Wingate AD, Campbell DG, Peggie M, Arthur JS, (2006) Nur77 is phosphorylated in cells by RSK in response to mitogenic stimulation. Biochem J 393: 715-724.
70. Zhang T, Jia N, Fei E, Wang P, Liao Z, et al. (2007) Nurr1 is phosphorylated by ERK2 in vitro and its phosphorylation upregulates tyrosine hydroxylase expression in SH-SY5Y cells. Neurosci Lett 423: 118-122.
71. Riccio A, Ahn S, Davenport CM, Blendy JA, Ginty DD, (1999) Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286: 2358-2361.
72. Popovici C, Fallet M, Marguet D, Birnbaum D, Roubin R, (2006) Intracellular trafficking of LET-756, a fibroblast growth factor of C. elegans, is controlled by a balance of export and nuclear signals. Exp Cell Res 312: 1484-1495.
73. Horbinski C, Stachowiak MK, Higgins D, Finnegan SG, (2001) Polyethyleneimine-mediated transfection of cultured postmitotic neurons from rat sympathetic ganglia and adult human retina. BMC Neurosci 2: 2.