Notch/Neurogenin 3 Signalling is Involved in the Neuritogenic Actions of Oestradiol in Developing Hippocampal Neurones

Journal of Neuroendocrinology

Volumn 23, Issue 4, 2011, Pages 355-364

  Ruiz Palmero, I ^a   Simon Areces, J ^a   Garcia Segura, L M ^a   Arevalo, M A ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

G protein coupled oestrogen receptor; G protein coupled receptor 30; Hairy and enhancer of split 1; Notch; Oestrogen receptors

Indexed keywords

BRAIN RECEPTOR; ESTRADIOL; G PROTEIN RECEPTOR 30; NEUROGENIN 3; NOTCH RECEPTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; HIPPOCAMPUS; HORMONE ACTION; MALE; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELLS, CULTURED; ESTRADIOL; ESTROGEN ANTAGONISTS; GENE EXPRESSION PROFILING; HIPPOCAMPUS; HOMEODOMAIN PROTEINS; MICE; NERVE TISSUE PROTEINS; NEURONS; RECEPTORS, NOTCH; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 79952681064     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02110.x     Document Type: Article

References (37)

1. Bray SJ. Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 2006; 7: 678-689.
2. Kovall RA. More complicated than it looks: assembly of Notch pathway transcription complexes. Oncogene 2008; 27: 5099-5109.
3. Berezovska O, McLean P, Knowles R, Frosh M, Lu FM, Lux SE, Hyman BT. Notch1 inhibits neurite outgrowth in postmitotic primary neurons. Neuroscience 1999; 93: 433-439.
4. Sestan N, Artavanis-Tsakonas S, Rakic P. Contact-dependent inhibition of cortical neurite growth mediated by notch signaling. Science 1999; 286: 741-746.
5. Salama-Cohen P, Arevalo MA, Meier J, Grantyn R, Rodriguez-Tebar A. NGF controls dendrite development in hippocampal neurons by binding to p75(NTR) and modulating the cellular targets of notch. Mol Biol Cell 2005; 16: 339-347.
6. Bertrand N, Castro DS, Guillemot F. Proneural genes and the specification of neural cell types. Nat Rev Neurosci 2002; 3: 517-530.
7. Salama-Cohen P, Arevalo MA, Grantyn R, Rodriguez-Tebar A. Notch and NGF/p75(NTR) control dendrite morphology and the balance of excitatory/inhibitory synaptic input to hippocampal neurones through neurogenin 3. J Neurochem 2006; 97: 1269-1278.
8. Ferreira A, Caceres A. Estrogen-enhanced neurite growth: evidence for a selective induction of Tau and stable microtubules. J Neurosci 1991; 11: 392-400.
9. Woolley CS. Effects of oestradiol on hippocampal circuitry. Novartis Found Symp 2000; 230: 173-180.
10. Duenas M, Torres-Aleman I, Naftolin F, Garcia-Segura LM. Interaction of insulin-like growth factor-I and estradiol signaling pathways on hypothalamic neuronal differentiation. Neuroscience 1996; 74: 531-539.
11. Topalli I, Etgen AM. Insulin-like growth factor-I receptor and estrogen receptor crosstalk mediates hormone-induced neurite outgrowth in PC12 cells. Brain Res 2004; 1030: 116-124.
12. Brito VI, Carrer HF, Cambiasso MJ. Inhibition of tyrosine kinase receptor type B synthesis blocks axogenic effect of estradiol on rat hypothalamic neurones in vitro. Eur J Neurosci 2004; 20: 331-337.
13. Beyer C, Karolczak M. Estrogenic stimulation of neurite growth in midbrain dopaminergic neurons depends on cAMP/protein kinase A signalling. J Neurosci Res 2000; 59: 107-116.
14. Gorosito SV, Cambiasso MJ. Axogenic effect of estrogen in male rat hypothalamic neurons involves Ca(2+), protein kinase C, and extracellular signal-regulated kinase signaling. J Neurosci Res 2008; 86: 145-157.
15. Minano A, Xifro X, Perez V, Barneda-Zahonero B, Saura CA, Rodriguez-Alvarez J. Estradiol facilitates neurite maintenance by a Src/Ras/ERK signalling pathway. Mol Cell Neurosci 2008; 39: 143-151.
16. Fitzgerald K, Harrington A, Leder P. Ras pathway signals are required for notch-mediated oncogenesis. Oncogene 2000; 19: 4191-4198.
17. Sharma N, Jadhav SP, Bapat SA. CREBBP re-arrangements affect protein function and lead to aberrant neuronal differentiation. Differentiation 2010; 79: 218-231.
18. Sundaram MV. RTK/Ras/MAPK signaling. WormBook 2006; February 11: 1-19.
19. Bender RA, Zhou L, Wilkars W, Fester L, Lanowski JS, Paysen D, Konig A, Rune GM. Roles of 17β-estradiol involve regulation of reelin expression and synaptogenesis in the dentate gyrus. Cereb Cortex 2010; 20: 2895-2995.
20. Goslin K, Banker G. Experimental observations on the development of polarity by hippocampal neurons in culture. J Cell Biol 1989; 108: 1507-1516.
21. Brewer GJ, Torricelli JR, Evege EK, Price PJ. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 1993; 35: 567-576.
22. Sholl DA. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 1953; 87: 387-406.
23. Simon-Areces J, Membrive G, Garcia-Fernandez C, Garcia-Segura LM, Arevalo MA. Neurogenin 3 cellular and subcellular localization in the developing and adult hippocampus. J Comp Neurol 2010; 518: 1814-1824.
24. von Schassen C, Fester L, Prange-Kiel J, Lohse C, Huber C, Bottner M, Rune GM. Oestrogen synthesis in the hippocampus: role in axon outgrowth. J Neuroendocrinol 2006; 18: 847-856.
25. Chakrabarty A, Blacklock A, Svojanovsky S, Smith PG. Estrogen elicits dorsal root ganglion axon sprouting via a renin-angiotensin system. Endocrinology 2008; 149: 3452-3460.
26. Cambiasso MJ, Carrer HF. Nongenomic mechanism mediates estradiol stimulation of axon growth in male rat hypothalamic neurons in vitro. J Neurosci Res 2001; 66: 475-481.
27. Carrer HF, Cambiasso MJ. Sexual differentiation of the brain: genes, estrogen, and neurotrophic factors. Cell Mol Neurobiol 2002; 22: 479-500.
28. Audesirk T, Cabell L, Kern M, Audesirk G. beta-estradiol influences differentiation of hippocampal neurons in vitro through an estrogen receptor-mediated process. Neuroscience 2003; 121: 927-934.
29. Zhao L, O'Neill K, Brinton RD. Estrogenic agonist activity of ICI 182, 780 (Faslodex) in hippocampal neurons: implications for basic science understanding of estrogen signaling and development of estrogen modulators with a dual therapeutic profile. J Pharmacol Exp Ther 2006; 319: 1124-1132.
30. Langer G, Bader B, Meoli L, Isensee J, Delbeck M, Noppinger PR, Otto C. A critical review of fundamental controversies in the field of GPR30 research. Steroids 2010; 75: 603-610.
31. Olde B, Leeb-Lundberg LM. GPR30/GPER1: searching for a role in estrogen physiology. Trends Endocrinol Metab 2009; 20: 409-416.
32. Prossnitz ER, Oprea TI, Sklar LA, Arterburn JB. The ins and outs of GPR30: a transmembrane estrogen receptor. J Steroid Biochem Mol Biol 2008; 109: 350-353.
33. Prossnitz ER, Maggiolini M. Mechanisms of estrogen signaling and gene expression via GPR30. Mol Cell Endocrinol 2009; 308: 32-38.
34. Terasawa E, Noel SD, Keen KL. Rapid action of oestrogen in luteinising hormone-releasing hormone neurones: the role of GPR30. J Neuroendocrinol 2009; 21: 316-321.
35. Zhang B, Subramanian S, Dziennis S, Jia J, Uchida M, Akiyoshi K, Migliati E, Lewis AD, Vandenbark AA, Offner H, Hurn PD. Estradiol and G1 reduce infarct size and improve immunosuppression after experimental stroke. J Immunol 2010; 184: 4087-4094.
36. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 2005; 307: 1625-1630.
37. Kang L, Zhang X, Xie Y, Tu Y, Wang D, Liu Z, Wang ZY. Involvement of estrogen receptor variant ER-alpha36, not GPR30, in nongenomic estrogen signaling. Mol Endocrinol 2010; 24: 709-721.