Selective regulation of 14-3-3η in primary culture of cerebral cortical neurons and astrocytes during development
The 14‐3‐3 proteins exist predominantly in the brain and may play regulatory roles in cellular processes of growth, differentiation, survival, and apoptosis. The biological functions, however, of the various 14‐3‐3 isoforms (β, ϵ, η, γ, and ζ) in the brain remain unclear. We have reported previously...
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| Published in | Journal of neuroscience research Vol. 79; no. 1-2; pp. 114 - 118 |
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| Format | Journal Article |
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| Abstract | The 14‐3‐3 proteins exist predominantly in the brain and may play regulatory roles in cellular processes of growth, differentiation, survival, and apoptosis. The biological functions, however, of the various 14‐3‐3 isoforms (β, ϵ, η, γ, and ζ) in the brain remain unclear. We have reported previously upregulation of 14‐3‐3γ in ischemic astrocytes. In the present study, we report selective regulation of 14‐3‐3η in cultured cerebral cortical neurons and astrocytes during in vitro development. In cultured neurons, gene expression levels of 14‐3‐3η increase with culture age (0–10 days). Brain‐derived neurotrophic factor and neurotrophin‐3 upregulate 14‐3‐3η gene expression. In cultured astrocytes, 14‐3‐3η is downregulated with culture age (1–5 weeks). The gene expression level of 14‐3‐3η is not affected by scratch injury in astrocytes or by ischemia in neurons. These data suggest a possible role of 14‐3‐3η in growth and differentiation of neurons and astrocytes, indicating an intricate mechanism governing coordinated and well‐controlled developmental events in the brain to ensure normal neural functions. © 2004 Wiley‐Liss, Inc. |
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| AbstractList | The 14‐3‐3 proteins exist predominantly in the brain and may play regulatory roles in cellular processes of growth, differentiation, survival, and apoptosis. The biological functions, however, of the various 14‐3‐3 isoforms (β, ϵ, η, γ, and ζ) in the brain remain unclear. We have reported previously upregulation of 14‐3‐3γ in ischemic astrocytes. In the present study, we report selective regulation of 14‐3‐3η in cultured cerebral cortical neurons and astrocytes during in vitro development. In cultured neurons, gene expression levels of 14‐3‐3η increase with culture age (0–10 days). Brain‐derived neurotrophic factor and neurotrophin‐3 upregulate 14‐3‐3η gene expression. In cultured astrocytes, 14‐3‐3η is downregulated with culture age (1–5 weeks). The gene expression level of 14‐3‐3η is not affected by scratch injury in astrocytes or by ischemia in neurons. These data suggest a possible role of 14‐3‐3η in growth and differentiation of neurons and astrocytes, indicating an intricate mechanism governing coordinated and well‐controlled developmental events in the brain to ensure normal neural functions. © 2004 Wiley‐Liss, Inc. |
| Author | Qin, Lu Ye Fung, Yin-Wan Wendy Wang, Chen Ran Liu, Shuang Yu, Albert Cheung-Hoi Chen, Xiao Qian |
| Author_xml | – sequence: 1 givenname: Xiao Qian surname: Chen fullname: Chen, Xiao Qian organization: Neuroscience Research Institute, Peking University, Key Laboratory of Neuroscience (Peking University), Ministry of Education, Department of Neurobiology, Peking University Health Science Center, Beijing, China – sequence: 2 givenname: Shuang surname: Liu fullname: Liu, Shuang organization: Neuroscience Research Institute, Peking University, Key Laboratory of Neuroscience (Peking University), Ministry of Education, Department of Neurobiology, Peking University Health Science Center, Beijing, China – sequence: 3 givenname: Lu Ye surname: Qin fullname: Qin, Lu Ye organization: Neuroscience Research Institute, Peking University, Key Laboratory of Neuroscience (Peking University), Ministry of Education, Department of Neurobiology, Peking University Health Science Center, Beijing, China – sequence: 4 givenname: Chen Ran surname: Wang fullname: Wang, Chen Ran organization: Neuroscience Research Institute, Peking University, Key Laboratory of Neuroscience (Peking University), Ministry of Education, Department of Neurobiology, Peking University Health Science Center, Beijing, China – sequence: 5 givenname: Yin-Wan Wendy surname: Fung fullname: Fung, Yin-Wan Wendy organization: Neuroscience Research Institute, Peking University, Key Laboratory of Neuroscience (Peking University), Ministry of Education, Department of Neurobiology, Peking University Health Science Center, Beijing, China – sequence: 6 givenname: Albert Cheung-Hoi surname: Yu fullname: Yu, Albert Cheung-Hoi email: achy@bjmu.edu.cn organization: Neuroscience Research Institute, Peking University, Key Laboratory of Neuroscience (Peking University), Ministry of Education, Department of Neurobiology, Peking University Health Science Center, Beijing, China |
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| CitedBy_id | crossref_primary_10_1007_s12035_010_8142_4 crossref_primary_10_1016_j_mam_2016_10_004 crossref_primary_10_1007_s12264_023_01040_x crossref_primary_10_1016_j_bbrc_2011_01_107 crossref_primary_10_1016_j_semcdb_2011_08_005 crossref_primary_10_1186_s12974_015_0381_x crossref_primary_10_1002_jnr_23486 crossref_primary_10_1007_s11064_007_9317_x crossref_primary_10_1186_s13041_017_0331_x crossref_primary_10_1007_s11064_017_2255_3 crossref_primary_10_1002_pmic_200600269 crossref_primary_10_1371_journal_pone_0009261 crossref_primary_10_1002_jcb_24254 crossref_primary_10_1002_jnr_21345 crossref_primary_10_1007_s11064_019_02717_4 crossref_primary_10_1007_s12035_020_02016_y crossref_primary_10_1002_prca_200800198 crossref_primary_10_1016_j_neuint_2009_02_016 crossref_primary_10_1111_jnc_12771 |
| Cites_doi | 10.1073/pnas.2131948100 10.1016/S0301-0082(03)00019-4 10.1002/glia.10185 10.1038/nrn1197 10.1002/bies.1134 10.1002/jnr.10742 10.1074/jbc.M005453200 10.1111/j.1471-4159.1986.tb00738.x 10.1074/jbc.M309620200 10.1038/sj.emboj.7600194 10.1146/annurev.biochem.72.121801.161629 10.1002/glia.1077 10.1523/JNEUROSCI.2528-03.2004 10.1093/emboj/cdg582 10.1523/JNEUROSCI.23-23-08212.2003 10.1023/A:1014871109943 10.1002/1097-4547(20001201)62:5<730::AID-JNR13>3.0.CO;2-K 10.1016/S0896-6273(02)01021-8 10.1002/jnr.490070104 10.1093/emboj/cdg545 10.1016/S0896-6273(04)00084-4 10.1016/S0197-0186(99)00145-X 10.1074/jbc.M201478200 10.1089/08977150151071035 10.1016/S0092-8674(03)00938-3 10.1523/JNEUROSCI.5209-03.2004 10.1016/S0006-291X(02)00895-1 10.1073/pnas.0308645100 10.1016/S0959-4388(00)00208-7 10.1523/JNEUROSCI.23-12-05050.2003 10.1016/0169-328X(93)90082-Z |
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| References | Yu ACH, Hertz L. 1982. Uptake of glutamate, GABA, and glutamine into a predominantly GABA-ergic and a predominantly glutamatergic nerve cell population in culture. J Neurosci Res 7: 23-35. Bulow HE, Hobert O. 2004. Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron 41: 723-736. Peng HB, Yang JF, Dai Z, Lee CW, Hung HW, Feng ZH, Ko CP. 2003. Differential effects of neurotrophins and Schwann cell-derived signals on neuronal survival/growth and synaptogenesis. J Neurosci 23: 5050-5060. Wu BY, Yu ACH. 2000. Quercetin inhibits c-fos, heat shock protein, and glial fibrillary acidic protein expression in injured astrocytes. J Neurosci Res 62: 730-736. Lau LT, Yu ACH. 2001. Astrocytes produce and release interleukin-1, interleukin-6, tumor necrosis factor alpha and interferon-gamma following traumatic and metabolic injury. J Neurotrauma 18: 351-359. Watanabe M, Isobe T, Ichimura T, Kuwano R, Takahashi Y, Kondo H. 1993. Molecular cloning of rat cDNAs for beta and gamma subtypes of 14-3-3 protein and developmental changes in expression of their mRNAs in the nervous system. Brain Res Mol Brain Res 17: 135-146. Yu ACH, Chan PH, Fishman RA. 1986. Effects of arachidonic acid on glutamate and gamma-aminobutyric acid uptake in primary cultures of rat cerebral cortical astrocytes and neurons. J Neurochem 47: 1181-1189. Gannon-Murakami L, Murakami K. 2002. Selective association of protein kinase C with 14-3-3 zeta in neuronally differentiated PC12 Cells. Stimulatory and inhibitory effect of 14-3-3 zeta in vivo. J Biol Chem 277: 23116-23122. Chang CW, Tsai CW, Wang HF, Tsai HC. 2004. Identification of a developmentally regulated striatum-enriched zinc-finger gene, Nolz-1, in the mammalian brain. Proc Natl Acad Sci USA 101: 2613-2618. Hekman M, Wiese S, Metz R, Albert S, Troppmair J, Nickel J, Sendtner M, Rapp UR. 2004. Dynamic changes in c-Raf phosphorylation and 14-3-3 protein binding in response to growth factor stimulation: differential roles of 14-3-3 protein binding sites. J Biol Chem 279: 14074-14086. Sadakata T, Mizoguchi A, Sato Y, Katoh-Semba R, Fukuda M, Mikoshiba K, Furuichi T. 2004. The secretory granule associated protein CAPS2 regulates neurotrophin release and cell survival. J Neurosci 24: 43-52. Chen XQ, Yu ACH. 2002. The association of 14-3-3γ and actin played a role in cell division and apoptosis in astrocytes. Biochem Biophys Res Commun 296: 657-663. Ma L, Harada T, Harada C, Romero M, Hebert JM, McConnell SK, Parada LF. 2002. Neurotrophin-3 is required for appropriate establishment of thalamocortical connections. Neuron 36: 623-634. Tsuruta F, Sunayama J, Mori Y, Hattori S, Shimizu S, Tsujimoto Y, Yoshioka K, Masuyama N, Gotoh Y. 2004. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J 23: 1889-1899. Barak O, Lazzaro MA, Lane WS, Speicher DW, Picketts DJ, Shiekhattar R. 2003. Isolation of human NURF: a regulator of Engrailed gene expression. EMBO J 22: 6089-6100. Berg D, Holzmann C, Riess O. 2003. 14-3-3 proteins in the nervous system. Nat Rev Neurosci 4: 752-762. Yu ACH, Wong HK, Yung HW, Lau LT. 2001. Ischemia-induced apoptosis in primary cultures of astrocytes. Glia 35: 121-130. Patapoutian A, Reichardt LF. 2001. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 11: 272-280. van Hemert MJ, Steensma HY, van Heusden GP. 2001. 14-3-3 proteins: key regulators of cell division, signalling and apoptosis. Bioessays 23: 936-946. Yu ACH, Lau LT. 2000. Expression of interleukin-1 alpha, tumor necrosis factor alpha and interleukin-6 genes in astrocytes under ischemic injury. Neurochem Int 36: 369-377. Itami C, Kimura F, Kohno T, Matsuoka M, Ichikawa M, Tsumoto T, Nakamura S. 2003. Brain-derived neurotrophic factor-dependent unmasking of "silent" synapses in the developing mouse barrel cortex. Proc Natl Acad Sci USA 100: 13069-13074. Li Q, Li Z, Sun CX, Yu ACH. 2002. Identification of transcripts expressed under functional differentiation in primary culture of cerebral cortical neurons. Neurochem Res 27: 147-154. Benton R, St. Johnston D. 2003. Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 115: 691-704. Huang EJ, Reichardt LF. 2003. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642. Kimura MT, Irie S, Shoji-Hoshino S, Mukai J, Nadano D, Oshimura M, Sato TA. 2001. 14-3-3 is involved in p75 neurotrophin receptor-mediated signal transduction. J Biol Chem 276: 17291-17300. Yu ACH, Yung HW, Hui MH, Lau LT, Chen XQ, Collins RA. 2003. Cyclohexamide and actinomycin D delay death and affect bcl-2, bax, and Ice gene expression in astrocytes under in vitro ischemia. J Neurosci Res 15: 318-325. Chen XQ, Chen JG, Zhang Y, Hsiao WW, Yu ACH. 2003. 14-3-3gamma is upregulated by in vitro ischemia and binds to protein kinase Raf in primary cultures of astrocytes. Glia 42: 315-324. Margolis SS, Walsh S, Weiser DC, Yoshida M, Shenolikar S, Kornbluth S. 2003. PP1 control of M phase entry exerted through 14-3-3-regulated Cdc25 dephosphorylation. EMBO J 22: 5734-5745. Saito A, Narasimhan P, Hayashi T, Okuno S, Ferrand-Drake M, Chan PH. 2004. Neuroprotective role of a proline-rich Akt substrate in apoptotic neuronal cell death after stroke: relationships with nerve growth factor. J Neurosci 24: 1584-1593. Burkhalter J, Fiumelli H, Allaman I, Chatton JY, Martin JL. 2003. Brain-derived neurotrophic factor stimulates energy metabolism in developing cortical neurons. J Neurosci 23: 8212-8220. Lessmann V, Gottmann K, Malcangio M. 2003. Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 69: 341-374. 2004; 101 2004; 41 2002; 36 2002; 296 2004; 23 2002; 277 2004; 24 2003; 15 2003; 115 2003; 72 2001; 23 2001; 276 2002; 27 2004; 279 1993; 17 2000; 36 1986; 47 2003; 69 2000; 62 2003; 4 1982; 7 2001; 18 2001; 11 2001; 35 2003; 42 2003; 100 2003; 22 2003; 23 e_1_2_5_27_1 e_1_2_5_28_1 e_1_2_5_25_1 e_1_2_5_26_1 e_1_2_5_23_1 e_1_2_5_24_1 e_1_2_5_21_1 e_1_2_5_22_1 e_1_2_5_29_1 e_1_2_5_20_1 e_1_2_5_15_1 e_1_2_5_14_1 e_1_2_5_17_1 e_1_2_5_9_1 e_1_2_5_16_1 e_1_2_5_8_1 e_1_2_5_11_1 e_1_2_5_7_1 e_1_2_5_10_1 e_1_2_5_6_1 e_1_2_5_13_1 e_1_2_5_32_1 e_1_2_5_5_1 e_1_2_5_12_1 e_1_2_5_4_1 e_1_2_5_3_1 e_1_2_5_2_1 e_1_2_5_19_1 e_1_2_5_18_1 e_1_2_5_30_1 e_1_2_5_31_1 |
| References_xml | – reference: Patapoutian A, Reichardt LF. 2001. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 11: 272-280. – reference: Barak O, Lazzaro MA, Lane WS, Speicher DW, Picketts DJ, Shiekhattar R. 2003. Isolation of human NURF: a regulator of Engrailed gene expression. EMBO J 22: 6089-6100. – reference: Berg D, Holzmann C, Riess O. 2003. 14-3-3 proteins in the nervous system. Nat Rev Neurosci 4: 752-762. – reference: Yu ACH, Yung HW, Hui MH, Lau LT, Chen XQ, Collins RA. 2003. Cyclohexamide and actinomycin D delay death and affect bcl-2, bax, and Ice gene expression in astrocytes under in vitro ischemia. J Neurosci Res 15: 318-325. – reference: Watanabe M, Isobe T, Ichimura T, Kuwano R, Takahashi Y, Kondo H. 1993. Molecular cloning of rat cDNAs for beta and gamma subtypes of 14-3-3 protein and developmental changes in expression of their mRNAs in the nervous system. Brain Res Mol Brain Res 17: 135-146. – reference: Huang EJ, Reichardt LF. 2003. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642. – reference: Gannon-Murakami L, Murakami K. 2002. Selective association of protein kinase C with 14-3-3 zeta in neuronally differentiated PC12 Cells. Stimulatory and inhibitory effect of 14-3-3 zeta in vivo. J Biol Chem 277: 23116-23122. – reference: Lessmann V, Gottmann K, Malcangio M. 2003. Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 69: 341-374. – reference: Chen XQ, Chen JG, Zhang Y, Hsiao WW, Yu ACH. 2003. 14-3-3gamma is upregulated by in vitro ischemia and binds to protein kinase Raf in primary cultures of astrocytes. Glia 42: 315-324. – reference: Itami C, Kimura F, Kohno T, Matsuoka M, Ichikawa M, Tsumoto T, Nakamura S. 2003. Brain-derived neurotrophic factor-dependent unmasking of "silent" synapses in the developing mouse barrel cortex. Proc Natl Acad Sci USA 100: 13069-13074. – reference: Saito A, Narasimhan P, Hayashi T, Okuno S, Ferrand-Drake M, Chan PH. 2004. Neuroprotective role of a proline-rich Akt substrate in apoptotic neuronal cell death after stroke: relationships with nerve growth factor. J Neurosci 24: 1584-1593. – reference: Chen XQ, Yu ACH. 2002. The association of 14-3-3γ and actin played a role in cell division and apoptosis in astrocytes. Biochem Biophys Res Commun 296: 657-663. – reference: Tsuruta F, Sunayama J, Mori Y, Hattori S, Shimizu S, Tsujimoto Y, Yoshioka K, Masuyama N, Gotoh Y. 2004. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J 23: 1889-1899. – reference: Peng HB, Yang JF, Dai Z, Lee CW, Hung HW, Feng ZH, Ko CP. 2003. Differential effects of neurotrophins and Schwann cell-derived signals on neuronal survival/growth and synaptogenesis. J Neurosci 23: 5050-5060. – reference: Lau LT, Yu ACH. 2001. Astrocytes produce and release interleukin-1, interleukin-6, tumor necrosis factor alpha and interferon-gamma following traumatic and metabolic injury. J Neurotrauma 18: 351-359. – reference: Wu BY, Yu ACH. 2000. Quercetin inhibits c-fos, heat shock protein, and glial fibrillary acidic protein expression in injured astrocytes. J Neurosci Res 62: 730-736. – reference: Bulow HE, Hobert O. 2004. Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron 41: 723-736. – reference: Hekman M, Wiese S, Metz R, Albert S, Troppmair J, Nickel J, Sendtner M, Rapp UR. 2004. Dynamic changes in c-Raf phosphorylation and 14-3-3 protein binding in response to growth factor stimulation: differential roles of 14-3-3 protein binding sites. J Biol Chem 279: 14074-14086. – reference: Sadakata T, Mizoguchi A, Sato Y, Katoh-Semba R, Fukuda M, Mikoshiba K, Furuichi T. 2004. The secretory granule associated protein CAPS2 regulates neurotrophin release and cell survival. J Neurosci 24: 43-52. – reference: Yu ACH, Lau LT. 2000. Expression of interleukin-1 alpha, tumor necrosis factor alpha and interleukin-6 genes in astrocytes under ischemic injury. Neurochem Int 36: 369-377. – reference: Ma L, Harada T, Harada C, Romero M, Hebert JM, McConnell SK, Parada LF. 2002. Neurotrophin-3 is required for appropriate establishment of thalamocortical connections. Neuron 36: 623-634. – reference: van Hemert MJ, Steensma HY, van Heusden GP. 2001. 14-3-3 proteins: key regulators of cell division, signalling and apoptosis. Bioessays 23: 936-946. – reference: Chang CW, Tsai CW, Wang HF, Tsai HC. 2004. Identification of a developmentally regulated striatum-enriched zinc-finger gene, Nolz-1, in the mammalian brain. Proc Natl Acad Sci USA 101: 2613-2618. – reference: Li Q, Li Z, Sun CX, Yu ACH. 2002. Identification of transcripts expressed under functional differentiation in primary culture of cerebral cortical neurons. Neurochem Res 27: 147-154. – reference: Yu ACH, Wong HK, Yung HW, Lau LT. 2001. Ischemia-induced apoptosis in primary cultures of astrocytes. Glia 35: 121-130. – reference: Benton R, St. Johnston D. 2003. Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 115: 691-704. – reference: Burkhalter J, Fiumelli H, Allaman I, Chatton JY, Martin JL. 2003. Brain-derived neurotrophic factor stimulates energy metabolism in developing cortical neurons. J Neurosci 23: 8212-8220. – reference: Kimura MT, Irie S, Shoji-Hoshino S, Mukai J, Nadano D, Oshimura M, Sato TA. 2001. 14-3-3 is involved in p75 neurotrophin receptor-mediated signal transduction. J Biol Chem 276: 17291-17300. – reference: Margolis SS, Walsh S, Weiser DC, Yoshida M, Shenolikar S, Kornbluth S. 2003. PP1 control of M phase entry exerted through 14-3-3-regulated Cdc25 dephosphorylation. EMBO J 22: 5734-5745. – reference: Yu ACH, Hertz L. 1982. 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| Title | Selective regulation of 14-3-3η in primary culture of cerebral cortical neurons and astrocytes during development |
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