The lin-4 microRNA targets the LIN-14 transcription factor to inhibit netrin-mediated axon attraction

Science Signaling

Volumn 5, Issue 228, 2012, Pages

  Zou, Yan ^a   Chiu, Hui ^a   Domenger, Dorothée ^b   Chuang, Chiou Fen ^a   Chang, Chieh ^a,b  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHEMOTACTIC FACTOR; ENA PROTEIN; GENE EXPRESSION MODULATOR 132; MADD 2 PROTEIN; MICRORNA; NETRIN; RAC1 PROTEIN; SLIT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LIN 14; TRANSCRIPTION FACTOR LIN 4; UNC 40 PROTEIN; UNC 6 PROTEIN; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CELL ADHESION MOLECULE; LIN 14 PROTEIN, C ELEGANS; LIN 4 MICRORNA, C ELEGANS; LIN-14 PROTEIN, C ELEGANS; LIN-4 MICRORNA, C ELEGANS; NERVE PROTEIN; NUCLEAR PROTEIN; PRIMER DNA; UNC 40 PROTEIN, C ELEGANS; UNC 6 PROTEIN, C ELEGANS; UNC-40 PROTEIN, C ELEGANS; UNC-6 PROTEIN, C ELEGANS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTERIOR LATERAL MICROTUBULE NEURON; ANTERIOR VENTRAL MICROTUBULE NEURON; ARTICLE; AXON ATTRACTION; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; GROWTH INHIBITION; LOSS OF FUNCTION MUTATION; MEDIATOR; MICROTUBULE; NERVE CELL; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; SIGNAL TRANSDUCTION; VENTRAL ROOT; VERTEBRATE; ANIMAL; DNA SEQUENCE; FLUORESCENCE MICROSCOPY; GENETICS; GROWTH CONE; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MOLECULAR GENETICS; MUTATION; NERVOUS SYSTEM DEVELOPMENT; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SEQUENCE ALIGNMENT; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; DNA PRIMERS; GROWTH CONES; LARVA; MICRORNAS; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; NEUROGENESIS; NUCLEAR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION;

EID: 84862536027     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002437     Document Type: Article

References (34)

1. C. Chang, T. W. Yu, C. I. Bargmann, M. Tessier-Lavigne, Inhibition of netrin-mediated axon attraction by a receptor protein tyrosine phosphatase. Science 305, 103-106 (2004).
2. R. C. Lee, R. L. Feinbaum, V. Ambros, The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854 (1993).
3. B. Wightman, I. Ha, G. Ruvkun, Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855-862 (1993).
4. B. J. Reinhart, F. J. Slack, M. Basson, A. E. Pasquinelli, J. C. Bettinger, A. E. Rougvie, H. R. Horvitz, G. Ruvkun, The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906 (2000).
5. G. Ruvkun, The perfect storm of tiny RNAs. Nat. Med. 14, 1041-1045 (2008).
6. R. J. Johnston, O. Hobert, A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426, 845-849 (2003).
7. S. Chang, R. J. Johnston Jr., C. Frøkjaer-Jensen, S. Lockery, O. Hobert, MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode. Nature 430, 785-789 (2004).
8. M. Boehm, F. Slack, A developmental timing microRNA and its target regulate life span in C. elegans. Science 310, 1954-1957 (2005).
9. J. E. Abrahante, A. L. Daul, M. Li, M. L. Volk, J. M. Tennessen, E. A. Miller, A. E. Rougvie, The Caenorhabditis elegans hunchback-like gene lin-57/hbl-1 controls developmental time and is regulated by microRNAs. Dev. Cell 4, 625-637 (2003).
10. S. Y. Lin, S. M. Johnson, M. Abraham, M. C. Vella, A. Pasquinelli, C. Gamberi, E. Gottlieb, F. J. Slack, The C. elegans hunchback homolog, hbl-1, controls temporal patterning and is a probable microRNA target. Dev. Cell 4, 639-650 (2003).
11. A. J. Giraldez, R. M. Cinalli, M. E. Glasner, A. J. Enright, J. M. Thomson, S. Baskerville, S. M. Hammond, D. P. Bartel, A. F. Schier, MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833-838 (2005).
12. T. F. Duchaine, J. A. Wohlschlegel, S. Kennedy, Y. Bei, D. Conte Jr., K. Pang, D. R. Brownell, S. Harding, S. Mitani, G. Ruvkun, J. R. Yates III, C. C. Mello, Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways. Cell 124, 343-354 (2006).
13. A. Grishok, A. E. Pasquinelli, D. Conte, N. Li, S. Parrish, I. Ha, D. L. Baillie, A. Fire, G. Ruvkun, C. C. Mello, Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106, 23-34 (2001).
14. C. Chen, D. A. Ridzon, A. J. Broomer, Z. Zhou, D. H. Lee, J. T. Nguyen, M. Barbisin, N. L. Xu, V. R. Mahuvakar, M. R. Andersen, K. Q. Lao, K. J. Livak, K. J. Guegler, Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 33, e179 (2005).
15. M. Lagos-Quintana, R. Rauhut, A. Yalcin, J. Meyer, W. Lendeckel, T. Tuschl, Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12, 735-739 (2002).
16. D. Banerjee, F. Slack, Control of developmental timing by small temporal RNAs: A paradigm for RNA-mediated regulation of gene expression. Bioessays 24, 119-129 (2002).
17. G. Ruvkun, J. Giusto, The Caenorhabditis elegans heterochronic gene lin-14 encodes a nuclear protein that forms a temporal developmental switch. Nature 338, 313-319 (1989).
18. M. Hristova, D. Birse, Y. Hong, V. Ambros, The Caenorhabditis elegans heterochronic regulator LIN-14 is a novel transcription factor that controls the developmental timing of transcription from the insulin/insulin-like growth factor gene ins-33 by direct DNA binding. Mol. Cell. Biol. 25, 11059-11072 (2005).
19. K. Fujisawa, J. L. Wrana, J. G. Culotti, The Slit receptor EVA-1 coactivates a SAX-3/Robo-mediated guidance signal in C. elegans. Science 317, 1934-1938 (2007).
20. S. Mitani, H. Du, D. H. Hall, M. Driscoll, M. Chalfie, Combinatorial control of touch receptor neuron expression in Caenorhabditis elegans. Development 119, 773-783 (1993).
21. F. J. Slack, M. Basson, Z. Liu, V. Ambros, H. R. Horvitz, G. Ruvkun, The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol. Cell 5, 659-669 (2000).
22. K. Olsson-Carter, F. J. Slack, The POU transcription factor UNC-86 controls the timing and ventral guidance of Caenorhabditis elegans axon growth. Dev. Dyn. 240, 1815-1825 (2011).
23. J. C. Hao, C. E. Adler, L. Mebane, F. B. Gertler, C. I. Bargmann, M. Tessier-Lavigne, The tripartite motif protein MADD-2 functions with the receptor UNC-40 (DCC) in Netrin-mediated axon attraction and branching. Dev. Cell 18, 950-960 (2010).
24. M. Alexander, G. Selman, A. Seetharaman, K. K. Chan, S. A. D'Souza, A. B. Byrne, P. J. Roy, MADD-2, a homolog of the Opitz syndrome protein MID1, regulates guidance to the midline through UNC-40 in Caenorhabditis elegans. Dev. Cell 18, 961-972 (2010).
25. E. A. Lundquist, P. W. Reddien, E. Hartwieg, H. R. Horvitz, C. I. Bargmann, Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development 128, 4475-4488 (2001).
26. Z. Gitai, T. W. Yu, E. A. Lundquist, M. Tessier-Lavigne, C. I. Bargmann, The Netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through Enabled and, in parallel, Rac and UNC-115/AbLIM. Neuron 37, 53-65 (2003).
27. C. Chang, C. E. Adler, M. Krause, S. G. Clark, F. B. Gertler, M. Tessier-Lavigne, C. I. Bargmann, MIG-10/lamellipodin and AGE-1/PI3K promote axon guidance and outgrowth in response to Slit and netrin. Curr. Biol. 16, 854-862 (2006).
28. C. C. Quinn, D. S. Pfeil, E. Chen, E. L. Stovall, M. V. Harden, M. K. Gavin, W. C. Forrester, E. F. Ryder, M. C. Soto, W. G. Wadsworth, UNC-6/netrin and SLT-1/slit guidance cues orient axon outgrowth mediated by MIG-10/RIAM/lamellipodin. Curr. Biol. 16, 845-853 (2006).
29. C. C. Quinn, D. S. Pfeil, W. G. Wadsworth, CED-10/Rac1 mediates axon guidance by regulating the asymmetric distribution of MIG-10/lamellipodin. Curr. Biol. 18, 808-813 (2008).
30. K. L. Goh, L. Cai, C. L. Cepko, F. B. Gertler, Ena/VASP proteins regulate cortical neuronal positioning. Curr. Biol. 12, 565-569 (2002).
31. S. Brenner, The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
32. C. Mello, A. Fire, DNA transformation. Methods Cell Biol. 48, 451-482 (1995).
33. C. Frøkjaer-Jensen, M. W. Davis, C. E. Hopkins, B. J. Newman, J. M. Thummel, S. P. Olesen, M. Grunnet, E. M. Jorgensen, Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40, 1375-1383 (2008).
34. B. J. Lesch, C. I. Bargmann, The homeodomain protein hmbx-1 maintains asymmetric gene expression in adult C. elegans olfactory neurons. Genes Dev. 24, 1802-1815 (2010).