5.9
CiteScore
5.9
Impact Factor
Volume 38 Issue 1
Jan.  2011
Turn off MathJax
Article Contents
Abstract
References
Article Navigation >  Journal of Genetics and Genomics  > 2011  >  38(1): 1-11

TRIM-9 functions in the UNC-6/UNC-40 pathway to regulate ventral guidance

doi: 10.1016/j.jcg.2010.12.004
  • a 

    Key Laboratory of Molecular and Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

  • b 

    State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

  • c 

    Graduate School of Chinese Academy of Sciences, Beijing 100049, China

More Information
  • Corresponding author: E-mail address: xhuang@genetics.ac.cn (Xun Huang)
  • Received Date: 2010-11-26
  • Accepted Date: 2010-12-07
  • Rev Recd Date: 2010-12-06
    • Available Online: 2011-02-19
  • Publish Date: 2011-01-20
    Abstract
  • TRIpartite Motif (TRIM) family proteins are ring finger domain-containing, multi-domain proteins implicated in many biological processes. Members of the TRIM-9/C-I subfamily of TRIM proteins, including TRIM-9, MID1 and MID2, have neuronal functions and are associated with neurological diseases. To explore whether the functions of C-I TRIM proteins are conserved in invertebrates, we analyzed Caenorhabditis elegans and Drosophila trim-9 mutants. C. elegans trim-9 mutants exhibit defects in the ventral guidance of hermaphrodite specific neuron (HSN) and the touch neuron AVM. Further genetic analyses indicate that TRIM-9 participates in the UNC-6-UNC-40 attraction pathway. Asymmetric distribution of UNC-40 during HSN development is normal in trim-9 mutants. However, the asymmetric localization of MIG-10, a downstream effector of UNC-40, is abolished in trim-9 mutants. These results suggest that TRIM-9 functions upstream of MIG-10 in the UNC-40 pathway. Moreover, we showed that TRIM-9 exhibits E3 ubiquitin ligase activity in vitro and this activity is important for TRIM-9 function in vivo. Additionally, we found that Drosophila trim-9 is required for the midline attraction of a group of sensory neuron axons. Over-expression of the Netrin/UNC-6 receptor Frazzled suppresses the guidance defects in trim-9 mutants. Our study reveals an evolutionarily conserved function of TRIM-9 in the UNC-40/Frazzled-mediated UNC-6/Netrin attraction pathway.
    • These authors contributed equally to this work.
    FullText(HTML)
    • References(43)
  • [1]
    Adler, C.E., Fetter, R.D., Bargmann, C.I. UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation Nat. Neurosci., 9 (2006),pp. 511-518
    [2]
    Ainsley, J.A., Pettus, J.M., Bosenko, D. et al. Curr. Biol., 13 (2003),pp. 1557-1563
    [3]
    Alexander, M., Selman, G., Seetharaman, A. et al. Dev. Cell, 18 (2010),pp. 961-972
    [4]
    Aranda-Orgilles, B., Aigner, J., Kunath, M. et al. Active transport of the ubiquitin ligase MID1 along the microtubules is regulated by protein phosphatase 2A PLoS ONE, 3 (2008),p. e3507
    [5]
    Berti, C., Messali, S., Ballabio, A. et al. TRIM9 is specifically expressed in the embryonic and adult nervous system Mech. Dev., 113 (2002),pp. 159-162
    [6]
    Brenner, S. Genetics, 77 (1974),pp. 71-94
    [7]
    Buchner, G., Montini, E., Andolfi, G. et al. MID2, a homologue of the Opitz syndrome gene MID1: similarities in subcellular localization and differences in expression during development Hum. Mol. Genet., 8 (1999),pp. 1397-1407
    [8]
    Chan, S.S., Zheng, H., Su, M.W. et al. Cell, 87 (1996),pp. 187-195
    [9]
    Chang, C., Adler, C.E., Krause, M. et al. MIG-10/lamellipodin and AGE-1/PI3K promote axon guidance and outgrowth in response to slit and netrin Curr. Biol., 16 (2006),pp. 854-862
    [10]
    Colavita, A., Culotti, J.G. Dev. Biol., 194 (1998),pp. 72-85
    [11]
    Dickson, B.J. Molecular mechanisms of axon guidance Science, 298 (2002),pp. 1959-1964
    [12]
    Drinjakovic, J., Jung, H., Campbell, D.S. et al. E3 ligase Nedd4 promotes axon branching by downregulating PTEN Neuron, 65 (2010),pp. 341-357
    [13]
    Gitai, Z., Yu, T.W., Lundquist, E.A. et al. The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/AbLIM Neuron, 37 (2003),pp. 53-65
    [14]
    Grill, B., Bienvenut, W.V., Brown, H.M. et al. Neuron, 55 (2007),pp. 587-601
    [15]
    Grueber, W.B., Ye, B., Moore, A.W. et al. Curr. Biol., 13 (2003),pp. 618-626
    [16]
    Hao, J.C., Adler, C.E., Mebane, L. et al. The tripartite motif protein MADD-2 functions with the receptor UNC-40 (DCC) in Netrin-mediated axon attraction and branching Dev. Cell, 18 (2010),pp. 950-960
    [17]
    Hedgecock, E.M., Culotti, J.G., Hall, D.H. Neuron, 4 (1990),pp. 61-85
    [18]
    Hu, G., Zhang, S., Vidal, M. et al. Genes Dev., 11 (1997),pp. 2701-2714
    [19]
    Huang, X., Cheng, H.J., Tessier-Lavigne, M. et al. MAX-1, a novel PH/MyTH4/FERM domain cytoplasmic protein implicated in netrin-mediated axon repulsion Neuron, 34 (2002),pp. 563-576
    [20]
    Huber, A.B., Kolodkin, A.L., Ginty, D.D. et al. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance Annu. Rev. Neurosci., 26 (2003),pp. 509-563
    [21]
    Jia, L., Emmons, S.W. Genetics, 173 (2006),pp. 1241-1258
    [22]
    Joazeiro, C.A., Weissman, A.M. RING finger proteins: mediators of ubiquitin ligase activity Cell, 102 (2000),pp. 549-552
    [23]
    Kawabe, H., Neeb, A., Dimova, K. et al. Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development Neuron, 65 (2010),pp. 358-372
    [24]
    Lancioni, A., Pizzo, M., Fontanella, B. et al. Lack of Mid1, the mouse ortholog of the Opitz syndrome gene, causes abnormal development of the anterior cerebellar vermis J. Neurosci., 30 (2010),pp. 2880-2887
    [25]
    Leung-Hagesteijn, C., Spence, A.M., Stern, B.D. et al. Cell, 71 (1992),pp. 289-299
    [26]
    Lewcock, J.W., Genoud, N., Lettieri, K. et al. The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics Neuron, 56 (2007),pp. 604-620
    [27]
    Li, H., Kulkarni, G., Wadsworth, W.G. J. Neurosci., 28 (2008),pp. 3595-3603
    [28]
    Li, Y., Chin, L.S., Weigel, C. et al. Spring, a novel RING finger protein that regulates synaptic vesicle exocytosis J. Biol. Chem., 276 (2001),pp. 40824-40833
    [29]
    Meroni, G., Diez-Roux, G. TRIM/RBCC, a novel class of ‘single protein RING finger’ E3 ubiquitin ligases Bioessays, 27 (2005),pp. 1147-1157
    [30]
    Nakata, K., Abrams, B., Grill, B. et al. Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development Cell, 120 (2005),pp. 407-420
    [31]
    Ozato, K., Shin, D.M., Chang, T.H. et al. TRIM family proteins and their emerging roles in innate immunity Nat. Rev. Immunol., 8 (2008),pp. 849-860
    [32]
    Quaderi, N.A., Schweiger, S., Gaudenz, K. et al. Opitz G/BBB syndrome, a defect of midline development, is due to mutations in a new RING finger gene on Xp22 Nat. Genet., 17 (1997),pp. 285-291
    [33]
    Quinn, C.C., Pfeil, D.S., Wadsworth, W.G. CED-10/Rac1 mediates axon guidance by regulating the asymmetric distribution of MIG-10/lamellipodin Curr. Biol., 18 (2008),pp. 808-813
    [34]
    Quinn, C.C., Pfeil, D.S., Chen, E. et al. UNC-6/netrin and SLT-1/slit guidance cues orient axon outgrowth mediated by MIG-10/RIAM/lamellipodin Curr. Biol., 16 (2006),pp. 845-853
    [35]
    Schweiger, S., Foerster, J., Lehmann, T. et al. The Opitz syndrome gene product, MID1, associates with microtubules Proc. Natl. Acad. Sci. USA, 96 (1999),pp. 2794-2799
    [36]
    Short, K.M., Cox, T.C. Subclassification of the RBCC/TRIM superfamily reveals a novel motif necessary for microtubule binding J. Biol. Chem., 281 (2006),pp. 8970-8980
    [37]
    Short, K.M., Hopwood, B., Yi, Z. et al. MID1 and MID2 homo- and heterodimerise to tether the rapamycin-sensitive PP2A regulatory subunit, alpha 4, to microtubules: implications for the clinical variability of X-linked Opitz GBBB syndrome and other developmental disorders BMC Cell Biol., 3 (2002),p. 1
    [38]
    Suzuki, M., Hara, Y., Takagi, C. et al. Development, 137 (2010),pp. 2329-2339
    [39]
    Sze, J.Y., Zhang, S., Li, J. et al. Development, 129 (2002),pp. 3901-3911
    [40]
    Tanji, K., Kamitani, T., Mori, F. et al. TRIM9, a novel brain-specific E3 ubiquitin ligase, is repressed in the brain of Parkinson’s disease and dementia with Lewy bodies Neurobiol. Dis., 38 (2010),pp. 210-218
    [41]
    Tessier-Lavigne, M., Goodman, C.S. The molecular biology of axon guidance Science, 274 (1996),pp. 1123-1133
    [42]
    Trockenbacher, A., Suckow, V., Foerster, J. et al. MID1, mutated in Opitz syndrome, encodes an ubiquitin ligase that targets phosphatase 2A for degradation Nat. Genet., 29 (2001),pp. 287-294
    [43]
    Zhen, M., Huang, X., Bamber, B. et al. Neuron, 26 (2000),pp. 331-343
    • Relative Articles

  • Relative Articles

    [1]Shuang Wu, Yiwei Zhang, Lan Yao, Jiaqiang Wang, Falong Lu, Yusheng Liu. m6A-modified RNAs possess distinct poly(A) tails[J]. Journal of Genetics and Genomics, 2023, 50(3): 208-211. doi: 10.1016/j.jgg.2022.10.001
    [2]Simranpreet Kaur, Nicole J. Van Bergen, Bruria Ben-Zeev, Emanuela Leonardi, Tiong Y. Tan, David Coman, Benjamin Kamien, Susan M. White, Miya St John, Dean Phelan, Kristin Rigbye, Sze Chern Lim, Michelle C. Torres, Melanie Marty, Elena Savva, Teresa Zhao, Sean Massey, Alessandra Murgia, Wendy A. Gold, John Christodoulou. Expanding the genetic landscape of Rett syndrome to include lysine acetyltransferase 6A (KAT6A)[J]. Journal of Genetics and Genomics, 2020, 47(10): 650-654. doi: 10.1016/j.jgg.2020.09.003
    [3]Zhe Sun, Ji-Long Liu. mTOR-S6K1 pathway mediates cytoophidium assembly[J]. Journal of Genetics and Genomics, 2019, 46(2): 65-74. doi: 10.1016/j.jgg.2018.11.006
    [4]Tao Tao, Jie Sun, Yajing Peng, Pei Wang, Xin Chen, Wei Zhao, Yeqiong Li, Lisha Wei, Wei Wang, Yanyan Zheng, Ye Wang, Xuena Zhang, Min-Sheng Zhu. Distinct functions of Trio GEF domains in axon outgrowth of cerebellar granule neurons[J]. Journal of Genetics and Genomics, 2019, 46(2): 87-96. doi: 10.1016/j.jgg.2019.02.003
    [5]Leilei Zheng, Zitong Zhao, Lulu Rong, Liyan Xue, Yongmei Song. RASSF6-TRIM16 axis promotes cell proliferation, migration and invasion in esophageal squamous cell carcinoma[J]. Journal of Genetics and Genomics, 2019, 46(10): 477-488. doi: 10.1016/j.jgg.2019.10.004
    [6]Sinian Xing, Meiru Jia, Lingzhi Wei, Wenwen Mao, Usman Ali Abbasi, Yaoyao Zhao, Yating Chen, Minglin Cao, Kai Zhang, Zhengrong Dai, Zhechao Dou, Wensuo Jia, Bingbing Li. CRISPR/Cas9-introduced single and multiple mutagenesis in strawberry[J]. Journal of Genetics and Genomics, 2018, 45(12): 685-687. doi: 10.1016/j.jgg.2018.04.006
    [7]Yongbiao Xue. The Chinese garden of genetics —celebrating 40th anniversary of Genetics Society of China[J]. Journal of Genetics and Genomics, 2018, 45(1): 1. doi: 10.1016/j.jgg.2018.01.005
    [8]Ying Zhang, Chi Xu, Yubo Han, Xiaofang Chen, Yan Zhang, Mingjie Xiao. The 10th National Congress of Genetic Society of China: Celebrating its 40th anniversary in Nanjing[J]. Journal of Genetics and Genomics, 2018, 45(12): 689-690. doi: 10.1016/j.jgg.2019.01.001
    [9]Yanni Li, Xu Li, Haisong Wang, Qian Gao, Jinxin Zhang, Wenhao Zhang, Zhisong Zhang, Luyuan Li, Yang Yu, Ling Shuai. CRISPR/Cas9-edited Pax6-GFP reporter system facilitates the generation of mouse neural progenitor cells during differentiation[J]. Journal of Genetics and Genomics, 2018, 45(5): 277-280. doi: 10.1016/j.jgg.2018.03.002
    [10]Yufeng Hua, Chun Wang, Jian Huang, Kejian Wang. A simple and efficient method for CRISPR/Cas9-induced mutant screening[J]. Journal of Genetics and Genomics, 2017, 44(4): 207-213. doi: 10.1016/j.jgg.2017.03.005
    [11]Changyan Chen, Shuai Yin, Wenze Cao, Margaret S. Ho. Drosophila ubiquitin E3 ligase dSmurf is required for synapse remodeling and axon pruning by glia[J]. Journal of Genetics and Genomics, 2017, 44(1): 67-70. doi: 10.1016/j.jgg.2016.10.007
    [12]Maximilian Haeussler, Jean-Paul Concordet. Genome Editing with CRISPR-Cas9: Can It Get Any Better?[J]. Journal of Genetics and Genomics, 2016, 43(5): 239-250. doi: 10.1016/j.jgg.2016.04.008
    [13]Jinjie Zhu, Ning Song, Silong Sun, Weilong Yang, Haiming Zhao, Weibin Song, Jinsheng Lai. Efficiency and Inheritance of Targeted Mutagenesis in Maize Using CRISPR-Cas9[J]. Journal of Genetics and Genomics, 2016, 43(1): 25-36. doi: 10.1016/j.jgg.2015.10.006
    [14]Yue Mei, Yan Wang, Huiqian Chen, Zhong Sheng Sun, Xing-Da Ju. Recent Progress in CRISPR/Cas9 Technology[J]. Journal of Genetics and Genomics, 2016, 43(2): 63-75. doi: 10.1016/j.jgg.2016.01.001
    [15]Renjie Jiao, Caixia Gao. The CRISPR/Cas9 Genome Editing Revolution[J]. Journal of Genetics and Genomics, 2016, 43(5): 227-228. doi: 10.1016/j.jgg.2016.05.004
    [16]Suhong Xu. The Application of CRISPR-Cas9 Genome Editing in Caenorhabditis elegans[J]. Journal of Genetics and Genomics, 2015, 42(8): 413-421. doi: 10.1016/j.jgg.2015.06.005
    [17]Chun Wang, Lan Shen, Yaping Fu, Changjie Yan, Kejian Wang. A Simple CRISPR/Cas9 System for Multiplex Genome Editing in Rice[J]. Journal of Genetics and Genomics, 2015, 42(12): 703-706. doi: 10.1016/j.jgg.2015.09.011
    [18]Andrew R. Bassett, Ji-Long Liu. CRISPR/Cas9 and Genome Editing in Drosophila[J]. Journal of Genetics and Genomics, 2014, 41(1): 7-19. doi: 10.1016/j.jgg.2013.12.004
    [19]Jiao Gao, Xin-Long Yan, Ren Li, Yi Liu, Wenyan He, Shengkun Sun, Yu Zhang, Bing Liu, Jiaxiang Xiong, Ning Mao. Characterization of OP9 as authentic mesenchymal stem cell line[J]. Journal of Genetics and Genomics, 2010, 37(7): 475-482. doi: 10.1016/S1673-8527(09)60067-9
    [20]Yushan Zhang, Hongli Du, Jing Chen, Guanfu Yang, Xiquan Zhang. Porcine growth differentiation factor 9 gene polymorphisms and their associations with litter size[J]. Journal of Genetics and Genomics, 2008, 35(3): 163-169. doi: 10.1016/S1673-8527(08)60022-3
    • Supplements(0)
    • Cited By
  • Created with Highcharts 5.0.7Amount of accessChart context menuAbstract Views, HTML Views, PDF Downloads StatisticsAbstract ViewsHTML ViewsPDF Downloads2024-062024-072024-082024-092024-102024-112024-122025-012025-022025-032025-042025-050123456
    Created with Highcharts 5.0.7Chart context menuAccess Class DistributionFULLTEXT: 19.5 %FULLTEXT: 19.5 %META: 79.7 %META: 79.7 %PDF: 0.8 %PDF: 0.8 %FULLTEXTMETAPDF
    Created with Highcharts 5.0.7Chart context menuAccess Area Distribution其他: 0.8 %其他: 0.8 %China: 50.8 %China: 50.8 %Russian Federation: 12.5 %Russian Federation: 12.5 %United States: 35.9 %United States: 35.9 %其他ChinaRussian FederationUnited States

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索
    Get Citation
    PDF

    Article Metrics

    Article views (101) PDF downloads (1) Cited by ()
    Proportional views
    Related

    Editorial Office

    Journal of Genetics and Genomics

    京ICP备09063187号-7

    No.1, West Beichen Road, Chaoyang District, Beijing 100101, P.R.China

    +86-10-64806528+86-10-64807786jgg@genetics.ac.cn

    Supported by: Beijing Renhe Information Technology Co. Ltd  

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return