An Optogenetic Method to Modulate Cell Contractility during Tissue Morphogenesis

Developmental Cell

Volumn 35, Issue 5, 2015, Pages 646-660

  Guglielmi, Giorgia ^a   Barry, Joseph D ^a,b   Huber, Wolfgang ^a   De Renzis, Stefano ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME 2; PROTEIN; PROTEIN CIB1; PROTEIN OCRL; SYNAPTOJANIN; UNCLASSIFIED DRUG; ACTIN; GREEN FLUORESCENT PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANISOTROPY; ARTICLE; CELL CONTRACTILITY; CELL FUNCTION; CELL INTERACTION; CELL MEMBRANE; CELL SHAPE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; ILLUMINATION; MORPHOGENESIS; NONHUMAN; OPTOGENETICS; PRIMORDIUM; PRIORITY JOURNAL; SINGLE PHOTON ILLUMINATION; TWO PHOTON ILLUMINATION; ANIMAL; CELL COMMUNICATION; CHEMISTRY; CONFOCAL MICROSCOPY; GENE EXPRESSION REGULATION; LIGHT; METABOLISM; MOLECULAR CLONING; PHOTON;

ACTINS; ANIMALS; ANISOTROPY; CELL COMMUNICATION; CELL MEMBRANE; CELL SHAPE; CLONING, MOLECULAR; DROSOPHILA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; LIGHT; MICROSCOPY, CONFOCAL; MORPHOGENESIS; OPTOGENETICS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOTONS;

EID: 84947725851     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.10.020     Document Type: Article

References (42)

1. Bardet P.L., Guirao B., Paoletti C., Serman F., Léopold V., Bosveld F., Goya Y., Mirouse V., Graner F., Bellaïche Y. PTEN controls junction lengthening and stability during cell rearrangement in epithelial tissue. Dev. Cell 2013, 25:534-546.
2. Barrett K., Leptin M., Settleman J. The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 1997, 91:905-915.
3. Behrndt M., Salbreux G., Campinho P., Hauschild R., Oswald F., Roensch J., Grill S.W., Heisenberg C.P. Forces driving epithelial spreading in zebrafish gastrulation. Science 2012, 338:257-260.
4. Bertet C., Sulak L., Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 2004, 429:667-671.
5. Comer F.I., Parent C.A. Phosphoinositides specify polarity during epithelial organ development. Cell 2007, 128:239-240.
6. Conte V., Muñoz J.J., Baum B., Miodownik M. Robust mechanisms of ventral furrow invagination require the combination of cellular shape changes. Phys. Biol. 2009, 6:016010.
7. Conte V., Ulrich F., Baum B., Muñoz J., Veldhuis J., Brodland W., Miodownik M. A biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo. PLoS ONE 2012, 7:e34473.
8. Denk W., Strickler J.H., Webb W.W. Two-photon laser scanning fluorescence microscopy. Science 1990, 248:73-76.
9. Fox D.T., Peifer M. Abelson kinase (Abl) and RhoGEF2 regulate actin organization during cell constriction in Drosophila. Development 2007, 134:567-578.
10. Giordano F., Saheki Y., Idevall-Hagren O., Colombo S.F., Pirruccello M., Milosevic I., Gracheva E.O., Bagriantsev S.N., Borgese N., De Camilli P. PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 2013, 153:1494-1509.
11. Harris T.J., Sawyer J.K., Peifer M. How the cytoskeleton helps build the embryonic body plan: models of morphogenesis from Drosophila. Curr. Top. Dev. Biol. 2009, 89:55-85.
12. Heisenberg C.P., Bellaïche Y. Forces in tissue morphogenesis and patterning. Cell 2013, 153:948-962.
13. Idevall-Hagren O., Dickson E.J., Hille B., Toomre D.K., De Camilli P. Optogenetic control of phosphoinositide metabolism. Proc. Natl. Acad. Sci. USA 2012, 109:E2316-E2323.
14. Irvine K.D., Wieschaus E. Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development 1994, 120:827-841.
15. Janetopoulos C., Devreotes P. Phosphoinositide signaling plays a key role in cytokinesis. J. Cell Biol. 2006, 174:485-490.
16. Kawano H., Kogure T., Abe Y., Mizuno H., Miyawaki A. Two-photon dual-color imaging using fluorescent proteins. Nat. Methods 2008, 5:373-374.
17. Kennedy M.J., Hughes R.M., Peteya L.A., Schwartz J.W., Ehlers M.D., Tucker C.L. Rapid blue-light-mediated induction of protein interactions in living cells. Nat. Methods 2010, 7:973-975.
18. Kölsch V., Seher T., Fernandez-Ballester G.J., Serrano L., Leptin M. Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 2007, 315:384-386.
19. Lecuit T., Lenne P.F., Munro E. Force generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 2011, 27:157-184.
20. Leptin M., Roth S. Autonomy and non-autonomy in Drosophila mesoderm determination and morphogenesis. Development 1994, 120:853-859.
21. Levskaya A., Weiner O.D., Lim W.A., Voigt C.A. Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 2009, 461:997-1001.
22. Liu H., Yu X., Li K., Klejnot J., Yang H., Lisiero D., Lin C. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 2008, 322:1535-1539.
23. Martin A.C., Goldstein B. Apical constriction: themes and variations on a cellular mechanism driving morphogenesis. Development 2014, 141:1987-1998.
24. Martin A.C., Kaschube M., Wieschaus E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 2009, 457:495-499.
25. Martin A.C., Gelbart M., Fernandez-Gonzalez R., Kaschube M., Wieschaus E.F. Integration of contractile forces during tissue invagination. J. Cell Biol. 2010, 188:735-749.
26. Mason F.M., Tworoger M., Martin A.C. Apical domain polarization localizes actin-myosin activity to drive ratchet-like apical constriction. Nat. Cell Biol. 2013, 15:926-936.
27. Mayer M., Depken M., Bois J.S., Jülicher F., Grill S.W. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 2010, 467:617-621.
28. McMahon A., Supatto W., Fraser S.E., Stathopoulos A. Dynamic analyses of Drosophila gastrulation provide insights into collective cell migration. Science 2008, 322:1546-1550.
29. Pelissier A., Chauvin J.P., Lecuit T. Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr. Biol. 2003, 13:1848-1857.
30. Putyrski M., Schultz C. Protein translocation as a tool: The current rapamycin story. FEBS Lett. 2012, 586:2097-2105.
31. Rauzi M., Verant P., Lecuit T., Lenne P.F. Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat. Cell Biol. 2008, 10:1401-1410.
32. Reversi A., Loeser E., Subramanian D., Schultz C., De Renzis S. Plasma membrane phosphoinositide balance regulates cell shape during Drosophila embryo morphogenesis. J. Cell Biol. 2014, 205:395-408.
33. Rozelle A.L., Machesky L.M., Yamamoto M., Driessens M.H., Insall R.H., Roth M.G., Luby-Phelps K., Marriott G., Hall A., Yin H.L. Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 2000, 10:311-320.
34. Sadler T.W., Greenberg D., Coughlin P., Lessard J.L. Actin distribution patterns in the mouse neural tube during neurulation. Science 1982, 215:172-174.
35. Sherrard K., Robin F., Lemaire P., Munro E. Sequential activation of apical and basolateral contractility drives ascidian endoderm invagination. Curr. Biol. 2010, 20:1499-1510.
36. Solon J., Kaya-Copur A., Colombelli J., Brunner D. Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 2009, 137:1331-1342.
37. Sweeton D., Parks S., Costa M., Wieschaus E. Gastrulation in Drosophila: the formation of the ventral furrow and posterior midgut invaginations. Development 1991, 112:775-789.
38. Toettcher J.E., Voigt C.A., Weiner O.D., Lim W.A. The promise of optogenetics in cell biology: interrogating molecular circuits in space and time. Nat. Methods 2011, 8:35-38.
39. Toettcher J.E., Weiner O.D., Lim W.A. Using optogenetics to interrogate the dynamic control of signal transmission by the Ras/Erk module. Cell 2013, 155:1422-1434.
40. Xie S., Martin A.C. Intracellular signalling and intercellular coupling coordinate heterogeneous contractile events to facilitate tissue folding. Nat. Commun. 2015, 6:7161.
41. Zallen J.A., Wieschaus E. Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell 2004, 6:343-355.
42. Zhang X., Jefferson A.B., Auethavekiat V., Majerus P.W. The protein deficient in Lowe syndrome is a phosphatidylinositol-4,5-bisphosphate 5-phosphatase. Proc. Natl. Acad. Sci. USA 1995, 92:4853-4856.