The p53 transcriptional target gene wnt7b contributes to NGF-inducible neurite outgrowth in neuronal PC12 cells

Differentiation

Volumn 76, Issue 7, 2008, Pages 795-808

  Brynczka, Christopher ^a,b,c   Merrick, B Alex ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Fzd; JNK; Neurite; NGF; p53; PC12; Wnt; Wnt7b

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BETA CATENIN; FRIZZLED PROTEIN; NERVE GROWTH FACTOR; PROTEIN P53; SECRETED FRIZZLED RELATED PROTEIN 1; SHORT HAIRPIN RNA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; WNT PROTEIN; WNT7B PROTEIN;

ANIMAL CELL; ARTICLE; CELL LEVEL; CELL STRAIN; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE OVEREXPRESSION; GENE TARGETING; GROWTH INHIBITION; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN TRANSPORT; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR CELL LINE; WNT7B GENE;

EID: 49749139763     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2007.00261.x     Document Type: Article

References (64)

1. Abu-Elmagd, M., Garcia-Morales, C. Wheeler, G.N. (2006) Frizzled7 mediates canonical Wnt signaling in neural crest induction. Dev Biol 298 : 285 298.
2. Akiyama, T. (2000) Wnt/beta-catenin signaling. Cytokine Growth Factor Rev 11 : 273 282.
3. Bacsi, A., Stanton, G.J., Hughes, T.K., Kruze, M. Boldogh, I. (2005) Colostrinin-driven neurite outgrowth requires p53 activation in PC12 cells. Cell Mol Neurobiol 25 : 1123 1139.
4. Brynczka, C., Labhart, P. Merrick, B.A. (2007) NGF-mediated transcriptional targets of p53 in PC12 neuronal differentiation. BMC Genom 8 : 139.
5. Brynczka, C. Merrick, B.A. (2007) Nerve growth factor potentiates p53 DNA binding but inhibits nitric oxide-induced apoptosis in neuronal PC12 cells. Neurochem Res 32 : 1572 1585.
6. Burrus, L.W. McMahon, A.P. (1995) Biochemical analysis of murine Wnt proteins reveals both shared and distinct properties. Exp Cell Res 220 : 363 373.
7. Caricasole, A., Ferraro, T., Iacovelli, L., Barletta, E., Caruso, A., Melchiorri, D., Terstappen, G.C. Nicoletti, F. (2003) Functional characterization of WNT7A signaling in PC12 cells: interaction with A FZD5 × LRP6 receptor complex and modulation by Dickkopf proteins. J Biol Chem 278 : 37024 37031.
8. Chan, S.L. Mattson, M.P. (1999) Caspase and calpain substrates: roles in synaptic plasticity and cell death. J Neurosci Res 58 : 167 190.
9. Chang, M.Y., Sun, W., Ochiai, W., Nakashima, K., Kim, S.Y., Park, C.H., Kang, J.S., Shim, J.W., Jo, A.Y., Kang, C.S., Lee, Y.S., Kim, J.S. Lee, S.H. (2007) Bcl-XL/Bax proteins direct the fate of embryonic cortical precursor cells. Mol Cell Biol 27 : 4293 4305.
10. Chen, X. Gumbiner, B.M. (2006) Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity. J Cell Biol 174 : 301 313.
11. Ciani, L. Salinas, P.C. (2005) WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci 6 : 351 362.
12. Coates, P.J., Lorimore, S.A., Lindsay, K.J. Wright, E.G. (2003) Tissue-specific p53 responses to ionizing radiation and their genetic modification: the key to tissue-specific tumour susceptibility? J Pathol 201 : 377 388.
13. Di Giovanni, S., Knights, C.D., Rao, M., Yakovlev, A., Beers, J., Catania, J., Avantaggiati, M.L. Faden, A.I. (2006) The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J 25 : 4084 4096.
14. di Masi, A., Antoccia, A., Dimauro, I., Argentino-Storino, A., Mosiello, A., Mango, R., Novelli, G. Tanzarella, C. (2006) Gene expression and apoptosis induction in p53-heterozygous irradiated mice. Mutat Res 594 : 49 62.
15. Donehower, L.A., Harvey, M., Slagle, B.L., McArthur, M.J., Montgomery, C.A.Jr., Butel, J.S. Bradley, A. (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356 : 215 221.
16. Eizenberg, O., Faber-Elman, A., 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.
17. Erdreich-Epstein, A. Shackleford, G.M. (1998) Differential expression of Wnt genes in normal and flat variants of PC12 cells, a cell line responsive to ectopic Wnt1 expression. Growth Factors 15 : 149 158.
18. Fabian, Z., Vecsernyes, M., Pap, M. Szeberenyi, J. (2006) The effects of a mutant p53 protein on the proliferation and differentiation of PC12 rat phaeochromocytoma cells. J Cell Biochem 99 : 1431 1441.
19. Fei, P., Bernhard, E.J. El-Deiry, W.S. (2002) Tissue-specific induction of p53 targets in vivo. Cancer Res 62 : 7316 7327.
20. Fokina, V.M. Frolova, E.I. (2006) Expression patterns of Wnt genes during development of an anterior part of the chicken eye. Dev Dyn 235 : 496 505.
21. Fujita, K., Lazarovici, P. Guroff, G. (1989) Regulation of the differentiation of PC12 pheochromocytoma cells. Env Health Perspect 80 : 127 142.
22. Gordon, M.D. Nusse, R. (2006) Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 281 : 22429 22433.
23. Gordon, S., Akopyan, G., Garban, H. Bonavida, B. (2006) Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25 : 1125 1142.
24. Hirabayashi, Y., Itoh, Y., Tabata, H., Nakajima, K., Akiyama, T., Masuyama, N. Gotoh, Y. (2004) The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131 : 2791 2801.
25. Hofmann, K. (2000) A superfamily of membrane-bound O-acyltransferases with implications for wnt signaling. Trends Biochem Sci 25 : 111 112.
26. Hughes, A.L., Gollapudi, L., Sladek, T.L. Neet, K.E. (2000) Mediation of nerve growth factor-driven cell cycle arrest in PC12 cells by p53. Simultaneous differentiation and proliferation subsequent to p53 functional inactivation. J Biol Chem 275 : 37829 37837.
27. Ille, F. Sommer, L. (2005) Wnt signaling: multiple functions in neural development. Cell Mol Life Sci 62 : 1100 1108.
28. Lee, D., Kim, J.W., Seo, T., Hwang, S.G., Choi, E.J. Choe, J. (2002) SWI/SNF complex interacts with tumor suppressor p53 and is necessary for the activation of p53-mediated transcription. J Biol Chem 277 : 22330 22337.
29. Lie, D.C., Colamarino, S.A., Song, H.J., Desire, L., Mira, H., Consiglio, A., Lein, E.S., Jessberger, S., Lansford, H., Dearie, A.R. Gage, F.H. (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437 : 1370 1375.
30. Logan, C.Y. Nusse, R. (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20 : 781 810.
31. Luo, J.L., Yang, Q., Tong, W.M., Hergenhahn, M., Wang, Z.Q. Hollstein, M. (2001) Knock-in mice with a chimeric human/murine p53 gene develop normally and show wild-type p53 responses to DNA damaging agents: a new biomedical research tool. Oncogene 20 : 320 328.
32. McMahon, A.P. Bradley, A. (1990) The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62 : 1073 1085.
33. McNeill-Blue, C., Wetmore, B.A., Sanchez, J.F., Freed, W.J. Merrick, B.A. (2006) Apoptosis mediated by p53 in rat neural AF5 cells following treatment with hydrogen peroxide and staurosporine. Brain Res 1112 : 1 15.
34. Mikels, A.J. Nusse, R. (2006) Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol 4 : e115.
35. Moumen, A., Masterson, P., O'Connor, M.J. Jackson, S.P. (2005) hnRNP K: an HDM2 target and transcriptional coactivator of p53 in response to DNA damage. Cell 123 : 1065 1078.
36. Naylor, S., Smalley, M.J., Robertson, D., Gusterson, B.A., Edwards, P.A. Dale, T.C. (2000) Retroviral expression of Wnt-1 and Wnt-7b produces different effects in mouse mammary epithelium. J Cell Sci 113 (Pt 12) : 2129 2138.
37. Nusse, R. (2005) Wnt signaling in disease and in development. Cell Res 15 : 28 32.
38. Parr, B.A., Cornish, V.A., Cybulsky, M.I. McMahon, A.P. (2001) Wnt7b regulates placental development in mice. Dev Biol 237 : 324 332.
39. Perez-Moreno, M. Fuchs, E. (2006) Catenins: keeping cells from getting their signals crossed. Dev Cell 11 : 601 612.
40. Pokroy, R., Tendler, Y., Pollack, A., Zinder, O. Weisinger, G. (2002) p53 expression in the normal murine eye. Invest Ophthalmol Vis Sci 43 : 1736 1741.
41. Poluha, W., Schonhoff, C.M., Harrington, K.S., Lachyankar, M.B., Crosbie, N.E., Bulseco, D.A. Ross, A.H. (1997) A novel, nerve growth factor-activated pathway involving nitric oxide, p53, and p21WAF1 regulates neuronal differentiation of PC12 cells. J Biol Chem 272 : 24002 24007.
42. Rawal, N., Castelo-Branco, G., Sousa, K.M., Kele, J., Kobayashi, K., Okano, H. Arenas, E. (2006) Dynamic temporal and cell type-specific expression of Wnt signaling components in the developing midbrain. Exp Cell Res 312 : 1626 1636.
43. Rosso, S.B., Sussman, D., Wynshaw-Boris, A. Salinas, P.C. (2005) Wnt signaling through dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 8 : 34 42.
44. Sah, V.P., Attardi, L.D., Mulligan, G.J., Williams, B.O., Bronson, R.T. Jacks, T. (1995) A subset of p53-deficient embryos exhibit exencephaly. Nat Genet 10 : 175 180.
45. Shu, W., Jiang, Y.Q., Lu, M.M. Morrisey, E.E. (2002) Wnt7b regulates mesenchymal proliferation and vascular development in the lung. Development 129 : 4831 4842.
46. Sui, G., Affar el, B., Shi, Y., Brignone, C., Wall, N.R., Yin, P., Donohoe, M., Luke, M.P., Calvo, D. Grossman, S.R. (2004) Yin Yang 1 is a negative regulator of p53. Cell 117 : 859 872.
47. Takahashi, M., Sato, K., Nomura, T. Osumi, N. (2002) Manipulating gene expressions by electroporation in the developing brain of mammalian embryos. Differentiation 70 : 155 162.
48. Tanaka, K., Kitagawa, Y. Kadowaki, T. (2002) Drosophila segment polarity gene product porcupine stimulates the posttranslational N-glycosylation of wingless in the endoplasmic reticulum. J Biol Chem 277 : 12816 12823.
49. Tanaka, K., Okabayashi, K., Asashima, M., Perrimon, N. Kadowaki, T. (2000) The evolutionarily conserved porcupine gene family is involved in the processing of the Wnt family. Eur J Biochem 267 : 4300 4311.
50. Thomas, K.R. Capecchi, M.R. (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346 : 847 850.
51. Tu, X., Joeng, K.S., Nakayama, K.I., Nakayama, K., Rajagopal, J., Carroll, T.J., McMahon, A.P. Long, F. (2007) Noncanonical Wnt signaling through G protein-linked PKCdelta activation promotes bone formation. Dev Cell 12 : 113 127.
52. Van Raay, T.J., Wang, Y.K., Stark, M.R., Rasmussen, J.T., Francke, U., Vetter, M.L. Rao, M.S. (2001) Frizzled 9 is expressed in neural precursor cells in the developing neural tube. Dev Genes Evol 211 : 453 457.
53. Veeman, M.T., Axelrod, J.D. Moon, R.T. (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5 : 367 377.
54. Vincan, E., Darcy, P.K., Farrelly, C.A., Faux, M.C., Brabletz, T. Ramsay, R.G. (2007) Frizzled-7 dictates three-dimensional organization of colorectal cancer cell carcinoids. Oncogene 26 : 2340 2352.
55. Vincan, E., Darcy, P.K., Smyth, M.J., Thompson, E.W., Thomas, R.J., Phillips, W.A. Ramsay, R.G. (2005) Frizzled-7 receptor ectodomain expression in a colon cancer cell line induces morphological change and attenuates tumor growth. Differentiation 73 : 142 153.
56. Vogelstein, B., Lane, D. Levine, A.J. (2000) Surfing the p53 network. Nature 408 : 307 310.
57. Vousden, K.H. (2006) Outcomes of p53 activation - spoilt for choice. J Cell Sci 119 : 5015 5020.
58. Wang, Z., Shu, W., Lu, M.M. Morrisey, E.E. (2005) Wnt7b activates canonical signaling in epithelial and vascular smooth muscle cells through interactions with Fzd1, Fzd10, and LRP5. Mol Cell Biol 25 : 5022 5030.
59. Weidenfeld, J., Shu, W., Zhang, L., Millar, S.E. Morrisey, E.E. (2002) The WNT7b promoter is regulated by TTF-1, GATA6, and Foxa2 in lung epithelium. J Biol Chem 277 : 21061 21070.
60. Wong, G.T., Gavin, B.J. McMahon, A.P. (1994) Differential transformation of mammary epithelial cells by Wnt genes. Mol Cell Biol 14 : 6278 6286.
61. Yi, F., Brubaker, P.L. Jin, T. (2005) TCF-4 mediates cell type-specific regulation of proglucagon gene expression by beta-catenin and glycogen synthase kinase-3beta. J Biol Chem 280 : 1457 1464.
62. Zhai, L., Chaturvedi, D. Cumberledge, S. (2004) Drosophila wnt-1 undergoes a hydrophobic modification and is targeted to lipid rafts, a process that requires porcupine. J Biol Chem 279 : 33220 33227.
63. Zhang, J., Yan, W. Chen, X. (2006) p53 is required for nerve growth factor-mediated differentiation of PC12 cells via regulation of TrkA levels. Cell Death Differ 13 : 2118 2128.
64. Zhao, C., Aviles, C., Abel, R.A., Almli, C.R., McQuillen, P. Pleasure, S.J. (2005) Hippocampal and visuospatial learning defects in mice with a deletion of frizzled 9, a gene in the Williams syndrome deletion interval. Development 132 : 2917 2927.