MiRNA-mediated feedback inhibition of JAK/STAT morphogen signalling establishes a cell fate threshold

Nature Cell Biology

Volumn 13, Issue 9, 2011, Pages 1062-1071

  Yoon, Wan Hee ^a   Meinhardt, Hans ^b   Montell, Denise J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APONTIC PROTEIN; BARBIE PROTEIN; JANUS KINASE; KEN PROTEIN; MICRORNA; MICRORNA 279; MORPHOGEN; STAT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL MIGRATION; CONTROLLED STUDY; DENSITY GRADIENT; DOWN REGULATION; DROSOPHILA; EMBRYO; ENZYME ACTIVITY; ENZYME REPRESSION; FEEDBACK SYSTEM; FEMALE; GAIN OF FUNCTION MUTATION; MEMBRANE POTENTIAL; NONHUMAN; OVARY FOLLICLE CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SHORT CIRCUIT CURRENT; SIGNAL TRANSDUCTION;

ALGORITHMS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL LINE; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEEDBACK, PHYSIOLOGICAL; FEMALE; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; JANUS KINASES; MALE; MICRORNAS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MUTATION; OOCYTES; OVARY; STAT TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 80052476313     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2316     Document Type: Article

References (36)

1. Silver, D. L. & Montell, D. J. Paracrine signaling through the JAK/STAT pathway activates invasive behavior of ovarian epithelial cells in Drosophila. Cell 107, 831-841 (2001). (Pubitemid 34084975)
2. Ghiglione, C. et al. The Drosophila cytokine receptor Domeless controls border cell migration and epithelial polarization during oogenesis. Development 129, 5437-5447 (2002). (Pubitemid 36033062)
3. Xi, R., McGregor, J. R. & Harrison, D. A. A gradient of JAK pathway activity patterns the anterior-posterior axis of the follicular epithelium. Dev. Cell 4, 167-177 (2003). (Pubitemid 36221794)
4. Starz-Gaiano, M., Melani, M., Wang, X., Meinhardt, H. & Montell, D. J. Feedback inhibition of Jak/STAT signaling by apontic is required to limit an invasive cell population. Dev. Cell 14, 726-738 (2008). (Pubitemid 351622614)
5. Driever, W. & Nusslein-Volhard, C. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54, 95-104 (1988).
6. Gould, A., Morrison, A., Sproat, G., White, R. A. & Krumlauf, R. Positive crossregulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 11, 900-913 (1997). (Pubitemid 27175296)
7. Gould, A., Itasaki, N. & Krumlauf, R. Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 21, 39-51 (1998). (Pubitemid 28355690)
8. Saka, Y. & Smith, J. C. A mechanism for the sharp transition of morphogen gradient interpretation in Xenopus. BMC Dev. Biol. 7, 47 (2007).
9. Ghiglione, C., Devergne, O., Cerezo, D. & Noselli, S. Drosophila RalA is essential for the maintenance of Jak/Stat signalling in ovarian follicles. EMBO Rep. 9, 676-682 (2008). (Pubitemid 351927689)
10. Silver, D. L., Geisbrecht, E. R. & Montell, D. J. Requirement for JAK/STAT signaling throughout border cell migration in Drosophila. Development 132, 3483-3492 (2005). (Pubitemid 41246122)
11. Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
12. Hornstein, E. & Shomron, N. Canalization of development by microRNAs. Nat. Genet. 38 (Suppl), S20-S24 (2006).
13. John, B. et al. Human microRNA targets. PLoS Biol. 2, e363 (2004).
14. Krek, A. et al. Combinatorial microRNA target predictions. Nat. Genet. 37, 495-500 (2005). (Pubitemid 40617277)
15. Lewis, B. P., Burge, C. B. & Bartel, D. P. Conserved seed pairing, often-anked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20 (2005). (Pubitemid 40094598)
16. Enright, A. J. et al. MicroRNA targets in Drosophila. Genome Biol. 5, R1 (2003).
17. Cayirlioglu, P. et al. Hybrid neurons in a microRNA mutant are putative evolutionary intermediates in insect CO2 sensory systems. Science 319, 1256-1260 (2008). (Pubitemid 351323024)
18. Ebert, M. S., Neilson, J. R. & Sharp, P. A. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 4, 721-726 (2007). (Pubitemid 47338166)
19. Loya, C. M., Lu, C. S., Van Vactor, D. & Fulga, T. A. Transgenic microRNA inhibition with spatiotemporal specificity in intact organisms. Nat. Methods 6, 897-903 (2009).
20. Bach, E. A. et al. GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr. Patterns 7, 323-331 (2007). (Pubitemid 44835275)
21. Starz-Gaiano, M., Melani, M., Meinhardt, H. & Montell, D. Interpretation of the UPD/JAK/STAT morphogen gradient in Drosophila follicle cells. Cell Cycle 8, 2917-2925 (2009).
22. Arbouzova, N. I., Bach, E. A. & Zeidler, M. P. Ken & barbie selectively regulates the expression of a subset of Jak/STAT pathway target genes. Curr. Biol. 16, 80-88 (2006). (Pubitemid 43049890)
23. Wang, X. et al. Analysis of cell migration using whole-genome expression profiling of migratory cells in the Drosophila ovary. Dev. Cell 10, 483-495 (2006).
24. Lukacsovich, T., Asztalos, Z., Juni, N., Awano, W. & Yamamoto, D. The Drosophila melanogaster 60A chromosomal division is extremely dense with functional genes: their sequences, genomic organization, and expression. Genomics 57, 43-56 (1999). (Pubitemid 29187935)
25. Castrillon, D. H. et al. Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster : characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135, 489-505 (1993). (Pubitemid 23307602)
26. Flaherty, M. S., Zavadil, J., Ekas, L. A. & Bach, E. A. Genome-wide expression profiling in the Drosophila eye reveals unexpected repression of notch signaling by the JAK/STAT pathway. Dev. Dyn. 238, 2235-2253 (2009).
27. Schier, A. F. Nodal morphogens. Cold Spring Harb. Perspect. Biol. 1, a003459 (2009).
28. Baksa, K., Parke, T., Dobens, L. L. & Dearolf, C. R. The Drosophila STAT protein, stat92E, regulates follicle cell differentiation during oogenesis. Dev. Biol. 243, 166-175 (2002). (Pubitemid 34208411)
29. Singh, S. R., Liu, W. & Hou, S. X. The adult Drosophila malpighian tubules are maintained by multipotent stem cells. Cell Stem. Cell 1, 191-203 (2007). (Pubitemid 47215591)
30. Gellon, G., Harding, K. W., McGinnis, N., Martin, M. M. & McGinnis, W. A genetic screen for modifiers of Deformed homeotic function identifies novel genes required for head development. Development 124, 3321-3331 (1997). (Pubitemid 27440447)
31. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461 (1999). (Pubitemid 29159845)
32. Rorth, P. et al. Systematic gain-of-function genetics in Drosophila. Development 125, 1049-1057 (1998).
33. Manseau, L. et al. GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev. Dyn. 209, 310-322 (1997). (Pubitemid 27282200)
34. Fischer, J. A., Giniger, E., Maniatis, T. & Ptashne, M. GAL4 activates transcription in Drosophila. Nature 332, 853-856 (1988).
35. Eulenberg, K. G. & Schuh, R. The tracheae defective gene encodes a bZIP protein that controls tracheal cell movement during Drosophila embryogenesis. EMBO J. 16, 7156-7165 (1997). (Pubitemid 27520813)
36. Pek, J. W., Lim, A. K. & Kai, T. Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev. Cell 17, 417-424 (2009).