JNK- and Rac1-dependent induction of immediate early gene pip92 suppresses neuronal differentiation

Journal of Neurochemistry

Volumn 100, Issue 2, 2007, Pages 555-566

  Park, Jung Bum ^a,b   Kim, Eun Joo ^a   Yang, Eun Jin ^a,c   Seo, Su Ryeon ^a   Chung, Kwang Chul ^a  

^a Yonsei University   (South Korea)

^b ATGen   (South Korea)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

c Jun N terminal kinase; Elk1; Immediate early gene; Neurite outgrowth; p21 activated kinase; Rac1; Rho1

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR ELK 1;

ANIMAL CELL; ARTICLE; BRAIN CELL; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; GENE ACTIVATION; GENE EXPRESSION; GENE INDUCTION; GENE REPRESSION; HIPPOCAMPUS; IMMEDIATE EARLY GENE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PIP92 GENE; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; BUTADIENES; CELL DEATH; CELL DIFFERENTIATION; CELLS, CULTURED; ENZYME INHIBITORS; HIPPOCAMPUS; IMMUNOPRECIPITATION; MAP KINASE KINASE 4; MAP KINASE KINASE KINASES; MICROINJECTIONS; MUTAGENESIS; NEURONS; NITRILES; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; RAC1 GTP-BINDING PROTEIN; RATS; RNA, SMALL INTERFERING; THYMIDINE KINASE; TRANSDUCTION, GENETIC; TRANSFECTION;

EID: 33845791508     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04263.x     Document Type: Article

References (49)

1. Benard V., Bohl B. P. and Bokoch G. M. (1999) Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274, 13 198-13 204.
2. Bortoff K. D., Zhu C. C., Hrywna Y. and Messina J. L. (1997) Insulin induction of pip92, CL-6, and novel mRNAs in rat hepatoma cells. Endocrine 7, 199-207.
3. Charles C. H., Simske J. S., O'Brien T. P. and Lau L. F. (1990) Pip92: a short-lived, growth factor-inducible protein in BALB/c 3T3 and PC12 cells. Mol. Cell Biol. 10, 6769-6774.
4. Chung K. C., Gomes I., Wang D., Lau L. F. and Rosner M. R. (1998) Raf and fibroblast growth factor phosphorylate Elk1 and activate the serum response element of the immediate early gene pip92 by mitogen-activated protein kinase-independent as well as -dependent signaling pathways. Mol. Cell Biol. 18, 2272-2281.
5. Chung K. C., Kim S. M., Rhang S., Lau L. F., Gomes I. and Ahn Y. S. (2000a) Expression of immediate early gene pip92 during anisomycin-induced cell death is mediated by the JNK- and p38-dependent activation of Elk1. Eur. J. Biochem. 267, 4676-4684.
6. Chung K. C., Shin S. W., Yoo M., Lee M. Y., Lee H. W., Choe B. K. and Ahn Y. S. (2000b) A systemic administration of NMDA induces immediate early gene pip92 in the hippocampus. J. Neurochem. 75, 9-17.
7. Chung K. C., Sung J. Y., Ahn W., Rhim H., Oh T. H., Lee M. G. and Ahn Y. S. (2001) Intracellular calcium mobilization induces immediate early gene pip92 via Src and mitogen-activated protein kinase in immortalized hippocampal cells. J. Biol. Chem. 276, 2132-2138.
8. Coleclough C., Kuhn L. and Lefkovits I. (1990) Regulation of mRNA abundance in activated T lymphocytes: identification of mRNA species affected by the inhibition of protein synthesis. Proc. Natl Acad. Sci. USA 87, 1753-1757.
9. Corbit K. C., Soh J. W., Yoshida K., Eves E. M., Weinstein I. B. and Rosner M. R. (2000) Different protein kinase C isoforms determine growth factor specificity in neuronal cells. Mol. Cell Biol. 20, 5392-5403.
10. Coso O. A., Chiariello M., Yu J. C., Teramoto H., Crespo P., Xu N., Miki T. and Gutkind J. S. (1995) The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146.
11. Daniels R. H., Hall P. S. and Bokoch G. M. (1998) Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J. 17, 754-764.
12. Etienne-Manneville S. and Hall A. (2002) Rho GTPases in cell biology. Nature 420, 629-635.
13. Eves E. M., Xiong W., Bellacosa A., Kennedy S. G., Tsichlis P. N., Rosner M. R. and Hay N. (1998) Akt, a target of phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neuronal cell line. Mol. Cell Biol. 18, 2143-2152.
14. Eves E. M., Skoczylas C., Yoshida K., Alnemri E. S. and Rosner M. R. (2001) FGF induces a switch in death receptor pathways in neuronal cells. J. Neurosci. 21, 4996-5006.
15. Ferreira A. and Kosik K. S. (1996) Accelerated neuronal differentiation induced by p53 suppression. J. Cell Sci. 109, 1509-1516.
16. Frost J. A., Xu S., Hutchison M. R., Marcus S. and Cobb M. H. (1996) Actions of Rho family small G proteins and p21-activated protein kinases on mitogen-activated protein kinase family members. Mol. Cell Biol. 16, 3707-3713.
17. Gille H., Strahl T. and Shaw P. E. (1995) Activation of ternary complex factor Elk-1 by stress-activated protein kinases. Curr. Biol. 5, 1191-1200.
18. Govek E. E., Newey S. E. and Van Aelst L. (2005) The role of the Rho GTPases in neuronal development. Genes Dev. 19, 1-49.
19. Hayashi K., Ohshima T. and Mikoshiba K. (2002) Pak1 is involved in dendrite initiation as a downstream effector of Rac1 in cortical neurons. Mol. Cell Neurosci. 20, 579-594.
20. Janknecht R., Ernst W. H., Pingoud V. and Nordheim A. (1993) Activation of ternary complex factor Elk-1 by MAP kinases. EMBO J. 12, 5097-5104.
21. Keeton A. B., Amsler M. O., Venable D. Y. and Messina J. L. (2002) Insulin signal transduction pathways and insulin-induced gene expression. J. Biol. Chem. 277, 48 565-48 573.
22. Kim M. S., Kim C. J., Jung H. S., Seo M. R., Juhnn Y. S., Shin H. Y., Ahn H. S., Thiele C. J. and Chi J. G. (2004) Fibroblast growth factor 2 induces differentiation and apoptosis of Askin tumour cells. J. Pathol. 202, 103-112.
23. Kozma R., Sarner S., Ahmed S. and Lim L. (1997) Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell Biol. 17, 1201-1211.
24. Kuo W. L., Abe M., Rhee J., Eves E. M., McCarthy S. A., Yan M., Templeton D. J., McMahon M. and Rosner M. R. (1996) Raf, but not MEK or ERK, is sufficient for differentiation of hippocampal neuronal cells. Mol. Cell Biol. 16, 1458-1470.
25. Kuo W. L., Chung K. C. and Rosner M. R. (1997) Differentiation of central nervous system neuronal cells by fibroblast-derived growth factor requires at least two signaling pathways: roles for Ras and Src. Mol. Cell Biol. 17, 4633-4643.
26. Latinkic B. V. and Lau L. F. (1994) Transcriptional activation of the immediate early gene pip92 by serum growth factors requires both Ets and CArG-like elements. J. Biol. Chem. 269, 23 163-23 170.
27. Latinkic B. V., Zeremski M. and Lau L. F. (1996) Elk-1 can recruit SRF to form a ternary complex upon the serum response element. Nucleic Acids Res. 24, 1345-1351.
28. Leeuwen F. N., Kain H. E., Kammen R. A., Michiels F., Kranenburg O. W. and Collard J. G. (1997) The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho. J. Cell Biol. 139, 797-807.
29. Li F., Adam L., Vadlamudi R. K., Zhou H., Sen S., Chernoff J., Mandal M. and Kumar R. (2002) p21-activated kinase 1 interacts with and phosphorylates histone H3 in breast cancer cells. EMBO Rep. 3, 767-773.
30. Liu D. X. and Greene L. A. (2001) Neuronal apoptosis at the G1/S cell cycle checkpoint. Cell Tissue Res. 305, 217-228.
31. Luo L. (2000) Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1, 173-180.
32. Manser E., Chong C., Zhao Z. S., Leung T., Michael G., Hall C. and Lim L. (1995) Molecular cloning of a new member of the p21-Cdc42/Rac-activated kinase (PAK) family. J. Biol. Chem. 270, 25 070-25 078.
33. Marais R., Wynne J. and Treisman R. (1993) The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell 73, 381-393.
34. Murga C., Zohar M., Teramoto H. and Gutkind J. S. (2002) Rac1 and RhoG promote cell survival by the activation of PI3K and Akt, independently of their ability to stimulate JNK and NF-κB. Oncogene 21, 207-216.
35. Nathans D., Lau L. F., Christy B., Hartzell S., Nakabeppu Y. and Ryder K. (1988) Genomic response to growth factors. Cold Spring Harb. Symp. Quant. Biol. 53, 893-900.
36. Nikolic M. (2002) The role of Rho GTPases and associated kinases in regulating neurite outgrowth. Int. J. Biochem. Cell Biol. 34, 731-745.
37. Nishida M., Nagao T. and Kurose H. (1999) Activation of Rac1 increases c-Jun NH(2)-terminal kinase activity and DNA fragmentation in a calcium-dependent manner in rat myoblast cell line H9c2. Biochem. Biophys. Res. Commun. 262, 350-354.
38. Park D. S., Morris E. J., Padmanabhan J., Shelanski M. L., Geller H. M. and Greene L. A. (1998) Cyclin-dependent kinases participate in death of neurons evoked by DNA-damaging agents. J. Cell Biol. 143, 457-467.
39. Parrini M. C., Matsuda M. and de Gunzburg J. (2005) Spatiotemporal regulation of the Pak1 kinase. Biochem. Soc. Trans. 33, 646-648.
40. Pearson G., Robinson F., Beers-Gibson T., Xu B. E., Karandikar M., Berman K. and Cobb M. H. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22, 153-183.
41. Ridley A. J. (2001) Rho family proteins: coordinating cell responses. Trends Cell Biol. 11, 471-477.
42. Schaeffer H. J. and Weber M. J. (1999) Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell Biol. 19, 2435-2444.
43. Schneider A., Fischer A., Weber D. et al. (2004) Restriction-mediated differential display (RMDD) identifies pip92 as a pro-apoptotic gene product induced during focal cerebral ischemia. J. Cereb. Blood Flow Metab. 24, 224-236.
44. Shimizu N., Ohta M., Fujiwara C., Sagara J., Mochizuki N., Oda T. and Utiyama H. (1991) Expression of a novel immediate early gene during 12-O-tetradecanoylphorbol-13-acetate-induced macrophagic differentiation of HL-60 cells. J. Biol. Chem. 266, 12 157-12 161.
45. Threadgill R., Bobb K. and Ghosh A. (1997) Regulation of dendritic growth and remodeling by Rho, Rac and Cdc42. Neuron 19, 625-634.
46. Tokuda H., Hirade K., Wang X., Oiso Y. and Kozawa O. (2003) Involvement of SAPK/JNK in basic fibroblast growth factor-induced vascular endothelial growth factor release in osteoblasts. J. Endocrinol. 177, 101-107.
47. Whitmarsh A. J., Shore P., Sharrocks A. D. and Davis R. J. (1995) Integration of MAP kinase signal transduction pathways at the serum response element. Science 269, 403-407.
48. Wong W. T., Faulkner-Jones B. E., Sanes J. R. and Wong R. O. (2000) Rapid dendritic remodeling in the developing retina: dependence on neurotransmission and reciprocal regulation by Rac and Rho. J. Neurosci. 20, 5024-5036.
49. Yang E. J., Ahn Y. S. and Chung K. C. (2001) Protein kinase Dyrk1 activates cAMP response element-binding protein during neuronal differentiation in hippocampal progenitor cells. J. Biol. Chem. 276, 39 819-39 824.