Estrogen induces neurite outgrowth via Rho family GTPases in neuroblastoma cells

Molecular and Cellular Neuroscience

Volumn 48, Issue 3, 2011, Pages 217-224

  Takahashi, Kazuhiro ^a   Piao, Shunai ^a   Yamatani, Hizuru ^a   Du, Botao ^a   Yin, Limei ^a   Ohta, Tsuyoshi ^a   Kawagoe, Jun ^a   Takata, Keiko ^a   Tsutsumi, Seiji ^a   Kurachi, Hirohisa ^a  

^a YAMAGATA UNIVERSITY   (Japan)

Author keywords

Cdc42; Estrogen; Medroxyprogesterone acetate; Neurite outgrowth; Rac1

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ANDROGEN RECEPTOR; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; GLUCOCORTICOID RECEPTOR; MEDROXYPROGESTERONE ACETATE; MIFEPRISTONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NERVE GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE; PROGESTERONE RECEPTOR; PROTEIN CDC42; PROTEIN KINASE B; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; CELL LINE; CELL STRUCTURE; CONTROLLED STUDY; CROSS LINKING; DRUG ANTAGONISM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ESTROGEN ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; NERVE FIBER GROWTH; NEUROBLASTOMA CELL; PRIORITY JOURNAL; REGULATORY MECHANISM;

CELL LINE, TUMOR; ESTRADIOL; HUMANS; MEDROXYPROGESTERONE ACETATE; MIFEPRISTONE; NEURITES; NEURONS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROGESTERONE; PROTO-ONCOGENE PROTEINS C-AKT; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 80053383256     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2011.08.002     Document Type: Article

References (55)

1. Andrade M.V., Hiragun T., Beaven M.A. Dexamethasone suppresses antigen-induced activation of phosphatidylinositol 3-kinase and downstream responses in mast cells. J. Immunol. 2004, 172:7254-7262.
2. Aoki K., Nakamura T., Matsuda M. Spatio-temporal regulation of Rac1 and Cdc42 activity during nerve growth factor-induced neurite outgrowth in PC12 cells. J. Biol. Chem. 2004, 279:713-719.
3. Bang O.Y., Hong H.S., Kim D.H., Kim H., Boo J.H., Huh K., Mook-Jung I. Neuroprotective effect of genistein against beta amyloid-induced neurotoxicity. Neurobiol. Dis. 2004, 16:21-28.
4. Barrie A.P., Clohessy A.M., Buensuceso C.S., Rogers M.V., Allen J.M. Pituitary adenylyl cyclase-activating peptide stimulates extracellular signal-regulated kinase 1 or 2 (ERK1/2) activity in a Ras-independent, mitogen-activated protein Kinase/ERK kinase 1 or 2-dependent manner in PC12 cells. J. Biol. Chem. 1997, 272:19666-19671.
5. Beyer C., Raab H. Nongenomic effects of oestrogen: embryonic mouse midbrain neurones respond with a rapid release of calcium from intracellular stores. Eur. J. Neurosci. 1998, 10:255-262.
6. Bi R., Foy M.R., Vouimba R.M., Thompson R.F., Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc. Natl. Acad. Sci. U. S. A 2001, 98:13391-13395.
7. Brinton R.D. A women's health issue: Alzheimer's disease and strategies for maintaining cognitive health. Int. J. Fertil. Womens. Med. 1999, 44:174-185.
8. Brownawell A.M., Kops G.J., Macara I.G., Burgering B.M. Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol. Cell. Biol. 2001, 21:3534-3546.
9. Burridge K., Wennerberg K. Rho and Rac take center stage. Cell 2004, 116167-116179.
10. Cambiasso M.J., Carrer H.F. Nongenomic mechanism mediates estradiol stimulation of axon growth in male rat hypothalamic neurons in vitro. J. Neurosci. Res. 2001, 66:475-481.
11. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr. Rev. 1999, 20:358-417.
12. da Silva J.S., Dotti C.G. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat. Rev. Neurosci. 2002, 3:694-704.
13. Dominguez R., Jalali C., de Lacalle S. Morphological effects of estrogen on cholinergic neurons in vitro involves activation of extracellular signal-regulated kinases. J. Neurosci. 2004, 24:982-990.
14. Du B., Ohmichi M., Takahashi K., Kawagoe J., Ohshima C., Igarashi H., Mori-Abe A., Saitoh M., Ohta T., Ohishi A., Doshida M., Tezuka N., Takahashi T., Kurachi H. Both estrogen and raloxifene protect against beta-amyloid-induced neurotoxicity in estrogen receptor alpha-transfected PC12 cells by activation of telomerase activity via Akt cascade. J. Endocrinol. 2004, 183:605-615.
15. Ferreira A., Caceres A. Estrogen-enhanced neurite growth: evidence for a selective induction of Tau and stable microtubules. J. Neurosci. 1991, 11:392-400.
16. Gambrell R.D. Prevention of endometrial cancer with progestogens. Maturitas 1986, 8:159-168.
17. Gollapudi L., Oblinger M.M. Estrogen effects on neurite outgrowth and cytoskeletal gene expression in ERalpha-transfected PC12 cell lines. Exp. Neurol. 2001, 171:308-316.
18. Govek E.E., Newey S.E., Van Aelst L. The role of the Rho GTPases in neuronal development. Genes Dev. 2005, 19:1-49.
19. Henderson V.W. Estrogen, cognition, and a woman's risk of Alzheimer's disease. Am. J. Med. 1997, 103:11S-18S.
20. Honda K., Sawada H., Kihara T., Urushitani M., Nakamizo T., Akaike A., Shimohama S. Phosphatidylinositol 3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. J. Neurosci. Res. 2000, 60:321-327.
21. Ivanova T., Mendez P., Garcia-Segura L.M., Beyer C. Rapid stimulation of the PI3-kinase/Akt signalling pathway in developing midbrain neurones by oestrogen. J. Neuroendocrinol. 2002, 14:73-79.
22. Kelly M.J., Levin E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab. 2001, 12:152-156.
23. Kim Y., Seger R., Suresh Babu C.V., Hwang S.Y., Yoo Y.S. A positive role of the PI3-K/Akt signaling pathway in PC12 cell differentiation. Mol. Cells. 2004, 18:353-359.
24. Koenig H.L., Gong W.H., Pelissier P. Role of progesterone in peripheral nerve repair. Rev. Reprod. 2000, 5:189-199.
25. Koubovec D., Ronacher K., Stubsrud E., Louw A., Hapgood J.P. Synthetic progestins used in HRT have different glucocorticoid agonist properties. Mol. Cell. Endocrinol. 2005, 242:23-32.
26. Maier C., Runzler D., Schindelar J., Grabner G., Waldhausl W., Kohler G., Luger A. G-protein-coupled glucocorticoid receptors on the pituitary cell membrane. J. Cell. Sci. 2005, 118:3353-3361.
27. Mannella P., Brinton R.D. Estrogen receptor protein interaction with phosphatidylinositol 3-kinase leads to activation of phosphorylated Akt and extracellular signal-regulated kinase 1/2 in the same population of cortical neurons: a unified mechanism of estrogen action. J. Neurosci. 2006, 26:9439-9447.
28. Melcangi R.C., Maggi R., Martini L. Testosterone and progesterone metabolism in the human neuroblastoma cell line SH-SY5Y. J. Steroid. Biochem. Mol. Biol. 1993, 46:811-818.
29. Mendez P., Azcoitia I., Garcia-Segura L.M. Estrogen receptor alpha forms estrogen-dependent multimolecular complexes with insulin-like growth factor receptor and phosphatidylinositol 3-kinase in the adult rat brain. Brain Res. Mol. Brain Res. 2003, 112:170-176.
30. Migliaccio A., Castoria G., Di Domenico M., de Falco A., Bilancio A., Lombardi M., Barone M.V., Ametrano D., Zannini M.S., Abbondanza C., Auricchio F. Steroid-induced androgen receptor-oestradiol receptor beta-Src complex triggers prostate cancer cell proliferation. EMBO J. 2000, 19:5406-5417.
31. Murdoch F.E., Gorski J. The role of ligand in estrogen receptor regulation of gene expression. Mol. Cell. Endocrinol. 1991, 78:C103-C188.
32. Nathan B.P., Barsukova A.G., Shen F., McAsey M., Strubl R.G. Estrogen facilitates neurite extension via apolipoprotein E in cultured adult mouse cortical neurons. Endocrinology 2004, 145:3065-3073.
33. Negishi M., Katoh H. Rho family GTPases as key regulators for neuronal network formation. J. Biochem. (Tokyo) 2002, 132:157-166.
34. Nilsen J., Mor G., Naftolin F. Raloxifene induces neurite outgrowth in estrogen receptor positive PC12 cells. Menopause 1998, 5:211-216.
35. Nilsen J., Brinton R.D. Impact of progestins on estrogen-induced neuroprotection: synergy by progesterone and 19-norprogesterone and antagonism by medroxyprogesterone acetate. Endocrinology 2002, 143:205-212.
36. Nilsen J., Brinton R.D. Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10506-10511.
37. Nusser N., Gosmanova E., Zheng Y., Tigyi G. Nerve growth factor signals through TrkA, phosphatidylinositol 3-kinase, and Rac1 to inactivate RhoA during the initiation of neuronal differentiation of PC12 cells. J. Biol. Chem. 2002, 277:35840-35846.
38. Ohmichi M., Pang L., Ribon V., Saltiel A.R. Divergence of signaling pathways for insulin in PC-12 pheochromocytoma cells. Endocrinology 1993, 133:6-56.
39. Oishi A., Takahashi K., Ohmichi M., Mochizuki Y., Inaba N., Kurachi H. Role of glucocorticoid receptor in the inhibitory effect of medroxyprogesterone acetate on the estrogen-induced endothelial nitric oxide synthase phosphorylation in human umbilical vein endothelial cells. Fertil. Steril. 2011, 95:1168-1170.
40. Razandi M., Pedram A., Levin E.R. Estrogen signals to the preservation of endothelial cell form and function. J. Biol. Chem. 2000, 275:38540-38546.
41. Razandi M., Pedram A., Rosen E.M., Levin E.R. BRCA1 inhibits membrane estrogen and growth factor receptor signaling to cell proliferation in breast cancer. Mol. Cell. Biol. 2004, 24:5900-5913.
42. Sarner S., Kozma R., Ahmed S., Lim L. Phosphatidylinositol 3-kinase, Cdc42, and Rac1 act downstream of Ras in integrin-dependent neurite outgrowth in N1E-115 neuroblastoma cells. Mol. Cell. Biol. 2000, 20:158-172.
43. Schafe G.E., Atkins C.M., Swank M.W., Bauer E.P., Sweatt J.D., LeDoux J.E. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. J. Neurosci. 2000, 20:8177-8187.
44. Shumaker S.A., Legault C., Rapp S.R., Thal L., Wallace R.B., Ockene J.K., Hendrix S.L., Jones B.N., Assaf A.R., Jackson R.D., Kotchen J.M., Wassertheil-Smoller S., Wactawski-Wende J., WHIMS Investigators Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 2003, 289:2651-2662.
45. Shumaker S.A., Legault C., Kuller L., Rapp S.R., Thal L., Lane D.S., Fillit H., Stefanick M.L., Hendrix S.L., Lewis C.E., Masaki K., Coker L.H. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004, 291:2947-2958. Women's Health Initiative Memory Study.
46. Simoncini T., Hafezi-Moghadam A., Brazil D.P., Ley K., Chin W.W., Liao J.K. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 2000, 407538-407541.
47. Sweatt J.D. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 2001, 76:1-10.
48. Topalli I., Etgen A.M. Insulin-like growth factor-I receptor and estrogen receptor crosstalk mediates hormone-induced neurite outgrowth in PC12 cells. Brain Res. 2004, 1030:116-124.
49. Wilson M.E., Liu Y., Wise P.M. Estradiol enhances Akt activation in cortical explant cultures following neuronal injury. Brain Res. Mol. Brain Res. 2002, 102:48-54.
50. Wyckoff M.H., Chambliss K.L., Mineo C., Yuhanna I.S., Mendelsohn M.E., Mumby S.M., Shaul P.W. Plasma membrane estrogen receptors are coupled to endothelial nitric-oxide synthase through Galpha(i). J. Biol. Chem. 2001, 276:27071-27076.
51. Yamaguchi Y., Katoh H., Yasui H., Mori K., Negishi M. RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J. Biol. Chem. 2001, 276:18977-18983.
52. Yankova M., Hart S.A., Woolley C.S. Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopic study. Proc. Natl. Acad. Sci. U. S. A 2001, 98:3525-3530.
53. Zhao L., Chen S., Ming Wang J., Brinton R.D. 17beta-estradiol induces Ca2+ influx, dendritic and nuclear Ca2+ rise and subsequent cyclic AMP response element-binding protein activation in hippocampal neurons: a potential initiation mechanism for estrogen neurotrophism. Neuroscience 2005, 132:299-311.
54. Zhang L., Rubinow D.R., Xaing G., Li B.S., Chang Y.H., Maric D., Barker J.L., Ma W. Estrogen protects against beta-amyloid-induced neurotoxicity in rat hippocampal neurons by activation of Akt. Neuroreport 2001, 12:1919-1923.
55. Znamensky V., Akama K.T., McEwen B.S., Milner T.A. Estrogen levels regulate the subcellular distribution of phosphorylated Akt in hippocampal CA1 dendrites. J. Neurosci. 2003, 23:2340-2347.