FoxO3a Negatively Regulates Nerve Growth Factor-Induced Neuronal Differentiation Through Inhibiting the Expression of Neurochondrin in PC12 Cells

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• 作者：Haitao Wang (1) (2)
  Xiaolu Duan (1) (2)
  Yannan Ren (1) (2)
  Yizhi Liu (2)
  Min Huang (1)
  Peiqing Liu (1)
  Rikang Wang (1) (2)
  Guoquan Gao (3)
  Lihua Zhou (3)
  Zhongping Feng (2)
  Wenhua Zheng (1) (2)
  
• 关键词：Neurochondrin ; FoxO3a ; Neurite outgrowth ; PI3K/Akt
• 刊名：Molecular Neurobiology
• 出版年：2013
• 出版时间：February 2013
• 年：2013
• 卷：47
• 期：1
• 页码：24-36
• 全文大小：503KB
• 参考文献：1. Ekoff M, Kaufmann T, Engstr?m M, Motoyama N, Villunger A, J?nsson JI, Strasser A, Nilsson G (2007) The BH3-only protein Puma plays an essential role in cytokine deprivation induced apoptosis of mast cells. Blood 110(9):3209-217 CrossRef
  2. Huang H, Tindall DJ (2007) Dynamic FoxO transcription factors. J Cell Sci 120(pt 15):2479-487 CrossRef
  3. Zheng WH, Kar S, Quirion R (2002) Insulin-like growth factor-1-induced phosphorylation of transcription factor FKHRL1 is mediated by phosphatidylinositol 3-kinase/Akt kinase and role of this pathway in insulin-like growth factor-1-induced survival of cultured hippocampal neurons. Mol Pharmacol 62(2):225-33 CrossRef
  4. Bakker WJ, Blázquez-Domingo M, Kolbus A, Besooyen J, Steinlein P, Beug H, Coffer PJ, L?wenberg B, von Lindern M, van Dijk TB (2004) FoxO3a regulates erythroid differentiation and induces BTG1, an activator of protein arginine methyl transferase 1. J Cell Biol 164(2):175-84 CrossRef
  5. Wen J, Xia Q, Wang C, Liu W, Chen Y, Gao J, Gong Y, Yin B, Ke Y, Qiang B, Yuan J, Peng X (2009) Dok-5 is involved in cardiomyocyte differentiation through PKB/FOXO3a pathway. J Mol Cell Cardiol 47(6):761-69 CrossRef
  6. Obermeier A, Bradshaw RA, Seedorf K, Choidas A, Schlessinger J, Ullrich A (1994) Neuronal differentiation signals are controlled by nerve growth factor receptor/Trk binding sites for SHC and PLC gamma. EMBO J 13(7):1585-590
  7. Vaudry D, Stork PJ, Lazarovici P, Eiden LE (2002) Signaling pathways for PC12 cell differentiation: making the right connections. Science 296(5573):1648-649 CrossRef
  8. Madduri S, Papalo?zos M, Gander B (2009) Synergistic effect of GDNF and NGF on axonal branching and elongation in vitro. Neurosci Res 65(1):88-7 CrossRef
  9. Pollock JD, Krempin M, Rudy B (1990) Differential effects of NGF, FGF, EGF, cAMP, and dexamethasone on neurite outgrowth and sodium channel expression in PC12 cells. J Neurosci 10(8):2626-637
  10. Drubin DG, Feinstein SC, Shooter EM, Kirschner MW (1985) Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors. J Cell Biol 101(5 pt 1):1799-807 CrossRef
  11. Zheng WH, Quirion R (2009) Glutamate acting on / N-methyl-d -aspartate receptors attenuates insulin-like growth factor-1 receptor tyrosine phosphorylation and its survival signaling properties in rat hippocampal neurons. J Biol Chem 284(2):855-61 CrossRef
  12. Dudgeon C, Wang P, Sun X, Peng R, Sun Q, Yu J, Zhang L (2010) PUMA induction by FoxO3a mediates the anticancer activities of the broad-range kinase inhibitor UCN-01. Mol Cancer Ther 9(11):2893-902 CrossRef
  13. Fu G, Peng C (2011) Nodal enhances the activity of FoxO3a and its synergistic interaction with Smads to regulate cyclin G2 transcription in ovarian cancer cells. Oncogene 30(37):3953-966 CrossRef
  14. Yoong LF, Too HP (2007) Glial cell line-derived neurotrophic factor and neurturin inhibit neurite outgrowth and activate RhoA through GFR alpha 2b, an alternatively spliced isoform of GFR alpha 2. J Neurosci 27(21):5603-614 CrossRef
  15. Tapley P, Lamballe F, Barbacid M (1992) K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 7(2):371-81
  16. Qian X, Riccio A, Zhang Y, Ginty DD (1998) Identification and characterization of novel substrates of Trk receptors in developing neurons. Neuron 21(5):1017-029 CrossRef
  17. Hur EM, Youssef S, Haws ME, Zhang SY, Sobel RA, Steinman L (2007) Osteopontin-induced relapse and progression of autoimmune brain disease through enhanced survival of activated T cells. Nat Immunol 8(1):74-3 CrossRef
  18. Mojsilovic-Petrovic J, Nedelsky N, Boccitto M, Mano I, Georgiades SN, Zhou W, Liu Y, Neve RL, Taylor JP, Driscoll M, Clardy J, Merry D, Kalb RG (2009) FOXO3a is broadly neuroprotective in vitro and in vivo against insults implicated in motor neuron diseases. J Neurosci 29(25):8236-247 CrossRef
  19. Picone P, Giacomazza D, Vetri V, Carrotta R, Militello V, San Biagio PL, Di Carlo M (2011) Insulin-activated Akt rescues Aβ oxidative stress-induced cell death by orchestrating molecular trafficking. Aging Cell 10(5):832-43 CrossRef
  20. Pirianov G, Brywe KG, Mallard C, Edwards AD, Flavell RA, Hagberg H, Mehmet H (2007) Deletion of the c-Jun / N-terminal kinase 3 gene protects neonatal mice against cerebral hypoxic-ischaemic injury. J Cereb Blood Flow Metab 27(5):1022-032
  21. Mao Z, Liu L, Zhang R, Li X (2007) Lithium reduces FoxO3a transcriptional activity by decreasing its intracellular content. Biol Psychiatry 62(12):1423-430 CrossRef
  22. Polter A, Yang S, Zmijewska AA, van Groen T, Paik JH, Depinho RA, Peng SL, Jope RS, Li X (2009) Forkhead box, class O transcription factors in brain: regulation and behavioral manifestation. Biol Psychiatry 65(2):150-59 CrossRef
  23. Cui M, Huang Y, Tian C, Zhao Y, Zheng J (2011) FOXO3a inhibits TNF-α- and IL-1β-induced astrocyte proliferation: implication for reactive astrogliosis. Glia 59(4):641-54 CrossRef
  24. Paik JH, Ding Z, Narurkar R, Ramkissoon S, Muller F, Kamoun WS, Chae SS, Zheng H, Ying H, Mahoney J, Hiller D, Jiang S, Protopopov A, Wong WH, Chin L, Ligon KL, DePinho RA (2009) FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5(5):540-53 CrossRef
  25. Renault VM, Rafalski VA, Morgan AA, Salih DA, Brett JO, Webb AE, Villeda SA, Thekkat PU, Guillerey C, Denko NC, Palmer TD, Butte AJ, Brunet A (2009) FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5(5):527-39 CrossRef
  26. Hoekman MF, Jacobs FM, Smidt MP, Burbach JP (2006) Spatial and temporal expression of FoxO transcription factors in the developing and adult murine brain. Gene Expr Patterns 6(2):134-40 CrossRef
  27. Song HJ, Stevens CF, Gage FH (2002) Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5(5):438-45
  28. Willaime-Morawek S, van der Kooy D (2008) Cortex- and striatum-derived neural stem cells produce distinct progeny in the olfactory bulb and striatum. Eur J Neurosci 27(9):2354-362 CrossRef
  29. Ferrón SR, Marqués-Torrejón MA, Mira H, Flores I, Taylor K, Blasco MA, Fari?as I (2009) Telomere shortening in neural stem cells disrupts neuronal differentiation and neuritogenesis. J Neurosci 29(46):14394-4407 CrossRef
  30. Teo JL, Ma H, Nguyen C, Lam C, Kahn M (2005) Specific inhibition of CBP/beta-catenin interaction rescues defects in neuronal differentiation caused by a presenilin-1 mutation. Proc Natl Acad Sci USA 102(34):12171-2176 CrossRef
  31. Bai Y, Cui M, Meng Z, Shen L, He Q, Zhang X, Chen F, Xiao J (2009) Ectopic expression of angiopoietin-1 promotes neuronal differentiation in neural progenitor cells through the Akt pathway. Biochem Biophys Res Commun 378(2):296-01 CrossRef
  32. Sinor AD, Lillien L (2004) Akt-1 expression level regulates CNS precursors. J Neurosci 24(39):8531-541 CrossRef
  33. Vojtek AB, Taylor J, DeRuiter SL, Yu JY, Figueroa C, Kwok RP, Turner DL (2003) Akt regulates basic helix-loop-helix transcription factor-coactivator complex formation and activity during neuronal differentiation. Mol Cell Biol 23(13):4417-427 CrossRef
  34. Eggert A, Ikegaki N, Liu X, Chou TT, Lee VM, Trojanowski JQ, Brodeur GM (2000) Molecular dissection of TrkA signal transduction pathways mediating differentiation in human neuroblastoma cells. Oncogene 19(16):2043-051 CrossRef
  35. Oishi K, Watatani K, Itoh Y, Okano H, Guillemot F, Nakajima K, Gotoh Y (2009) Selective induction of neocortical GABAergic neurons by the PDK1–Akt pathway through activation of Mash1. Proc Natl Acad Sci USA 106(31):13064-3069 CrossRef
  36. Mochizuki R, Dateki M, Yanai K, Ishizuka Y, Amizuka N, Kawashima H, Koga Y, Ozawa H, Fukamizu A (2003) Targeted disruption of the neurochondrin/norbin gene results in embryonic lethality. Biochem Biophys Res Commun 310(4):1219-226 CrossRef
  37. Istvánffy R, Vogt Weisenhorn DM, Floss T, Wurst W (2004) Expression of neurochondrin in the developing and adult mouse brain. Dev Genes Evol 214(4):206-09 CrossRef
  38. Shinozaki K, Maruyama K, Kume H, Kuzume H, Obata K (1997) A novel brain gene, norbin, induced by treatment of tetraethylammonium in rat hippocampal slice and accompanied with neurite-outgrowth in neuro 2a cells. Biochem Biophys Res Commun 240(3):766-71 CrossRef
  39. Schwaibold EM, Brandt DT (2008) Identification of neurochondrin as a new interaction partner of the FH3 domain of the diaphanous-related formin Dia1. Biochem Biophys Res Commun 373(3):366-72 CrossRef
  40. Ohoka Y, Hirotani M, Sugimoto H, Fujioka S, Furuyama T, Inagaki S (2001) Associates with a neurite-outgrowth-related protein, SFAP75. Biochem Biophys Res Commun 280(1):237-43 CrossRef
  41. Winner B, Melrose HL, Zhao C, Hinkle KM, Yue M, Kent C, Braithwaite AT, Ogholikhan S, Aigner R, Winkler J, Farrer MJ, Gage FH (2011) Adult neurogenesis and neurite outgrowth are impaired in LRRK2 G2019S mice. Neurobiol Dis 41(3):706-16 CrossRef
  42. Wang H, Westin L, Nong Y, Birnbaum S, Bendor J, Brismar H, Nestler E, Aperia A, Flajolet M, Greengard P (2009) Norbin is an endogenous regulator of metabotropic glutamate receptor 5 signaling. Science 326(5959):1554-557 CrossRef
  43. Shinozaki K, Kume H, Kuzume H, Obata K, Maruyama K (1999) Norbin, a neurite-outgrowth-related protein, is a cytosolic protein localized in the somatodendritic region of neurons and distributed prominently in dendritic outgrowth in Purkinje cells. Brain Res Mol Brain Res 71(2):364-68 CrossRef
  44. Van Pelt J, van Ooyen A, Corner MA (1996) Growth cone dynamics and activity-dependent processes in neuronal network development. Prog Brain Res 108:333-46 CrossRef
  
• 作者单位：Haitao Wang (1) (2)
  Xiaolu Duan (1) (2)
  Yannan Ren (1) (2)
  Yizhi Liu (2)
  Min Huang (1)
  Peiqing Liu (1)
  Rikang Wang (1) (2)
  Guoquan Gao (3)
  Lihua Zhou (3)
  Zhongping Feng (2)
  Wenhua Zheng (1) (2)
  
  1. Neuropharmacology, School of Pharmaceutical Sciences, Sun Yat-sen University, Guangzhou, 510006, China
  2. State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, 510006, China
  3. Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, 510006, China
  

文摘

Forkhead box O3 (FoxO3a) is a forkhead family transcription factor playing important roles in non-neuronal differentiation, metabolism, proliferation, and survival, but its role in neuronal differentiation remains unclear. In the present study, we investigated the role of FoxO3a in neuronal differentiation and its underlying mechanisms. Our results showed that overexpression of FoxO3a inhibited neuronal differentiation of PC12 cells induced by nerve growth factor (NGF) while knockdown of FoxO3a by siRNA enhanced NGF-induced differentiation. DNA microarray analysis and quantitative reverse transcription PCR (RT-PCR) showed that the overexpression of FoxO3a significantly attenuated expression of neurochondrin (NCDN), a neurite outgrowth-related protein, in PC12 cells, while knocking down the expression of FoxO3a had the opposite effect. Bioinformatic studies found that the regulatory region of NCDN promoter contained multiple FoxO3a binding sites. Dual-luciferase reporter assay with report gene containing NCDN promoter showed that FoxO3a significantly decreased the transcription activity of NCDN promoter. These results indicate that NCDN is a direct downstream target of FoxO3a which negatively regulates the expression of NCDN. Interestingly, NGF-induced NCDN expression and cell differentiation was blocked by the inhibition of phosphatidylinositol-3-kinase (PI3K)–protein kinase B (PKB, Akt) signal pathway (activation of FoxO3a) and overexpression of FoxO3a. Moreover, knockdown of NCDN by siRNA blocked NGF-induced neuronal differentiation of PC12 cells while overexpression of NCDN significantly promoted neurite outgrowth. These results put together demonstrate that NCDN plays an important role in NGF-induced neuronal differentiation and suggest that FoxO3a inhibits NGF-induced neuronal differentiation, at least in part, by suppressing the expression of NCDN.