The pros and cons of common actin labeling tools for visualizing actin dynamics during Drosophila oogenesis

Developmental Biology

Volumn 393, Issue 2, 2014, Pages 209-226

  Spracklen, Andrew J ^a   Fagan, Tiffany N ^a   Lovander, Kaylee E ^a   Tootle, Tina L ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Actin; Live Imaging; Oogenesis

Indexed keywords

F ACTIN; UTROPHIN; ACTIN; DROSOPHILA PROTEIN; GAL4 PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR;

ACTIN FILAMENT; ARTICLE; CELL NUCLEUS; CHROMOSOME INSERTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA; FEMALE; FEMALE FERTILITY; HETEROZYGOSITY; HIGH TEMPERATURE; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; OVARY FOLLICLE DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SOMATIC CELL; TEMPERATURE; ANIMAL; BIOSYNTHESIS; CONFOCAL MICROSCOPY; EMBRYOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OVARY FOLLICLE; PHYSIOLOGY; STAINING;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; MICROSCOPY, CONFOCAL; OOGENESIS; OVARIAN FOLLICLE; STAINING AND LABELING; TRANSCRIPTION FACTORS; UTROPHIN;

EID: 84908130576     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.06.022     Document Type: Article

References (60)

1. Abramoff M.D., Magalhaes P.J., Ram S.J. Image processing with ImageJ. Biophotonics Int. 2004, 11:36-42.
2. Aizawa H., Sameshima M., Yahara I. A green fluorescent protein-actin fusion protein dominantly inhibits cytokinesis, cell spreading, and locomotion in Dictyostelium. Cell Struct. Funct. 1997, 22:335-345.
3. Baarlink C., Wang H., Grosse R. Nuclear actin network assembly by formins regulates the SRF coactivator MAL. Science 2013, 340:864-867.
4. Belin B.J., Cimini B.A., Blackburn E.H., Mullins R.D. Visualization of actin filaments and monomers in somatic cell nuclei. Mol. Biol. Cell 2013, 24:982-994.
5. Boyle M.J., French R.L., Cosand K.A., Dorman J.B., Kiehart D.P., Berg C.A. Division of labor: subsets of dorsal-appendage-forming cells control the shape of the entire tube. Dev. Biol. 2010, 346:68-79.
6. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
7. Brock A.R., Wang Y., Berger S., Renkawitz-Pohl R., Han V.C., Wu Y., Galko M.J. Transcriptional regulation of Profilin during wound closure in Drosophila larvae. J. Cell Sci. 2012, 125:5667-5676.
8. Burkel B.M., von Dassow G., Bement W.M. Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil. Cytoskelet. 2007, 64:822-832.
9. Case L.B., Waterman C.M. Adhesive F-actin waves: a novel integrin-mediated adhesion complex coupled to ventral actin polymerization. PloS One 2011, 6:e26631.
10. Cooley L., Verheyen E., Ayers K. chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell 1992, 69:173-184.
11. Cox R.T., Spradling A.C. A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 2003, 130:1579-1590.
12. Deibler M., Spatz J.P., Kemkemer R. Actin fusion proteins alter the dynamics of mechanically induced cytoskeleton rearrangement. PloS One 2011, 6:e22941.
13. Duffy J.B. GAL4 system in Drosophila: a fly geneticist[U+05F3]s Swiss army knife. Genesis 2002, 34:1-15.
14. Edwards K.A., Demsky M., Montague R.A., Weymouth N., Kiehart D.P. GFP-moesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev. Biol. 1997, 191:103-117.
15. Gates J., Nowotarski S.H., Yin H., Mahaffey J.P., Bridges T., Herrera C., Homem C.C., Janody F., Montell D.J., Peifer M. Enabled and Capping protein play important roles in shaping cell behavior during Drosophila oogenesis. Dev. Biol. 2009, 333:90-107.
16. Groen C.M., Spracklen A.J., Fagan T.N., Tootle T.L. Drosophila Fascin is a novel downstream target of prostaglandin signaling during actin remodeling. Mol. Biol. Cell 2012, 23:4567-4578.
17. Grosse R., Vartiainen M.K. To be or not to be assembled: progressing into nuclear actin filaments. Nature reviews. Mol. Cell Biol. 2013, 14:693-697.
18. Guild G.M., Connelly P.S., Shaw M.K., Tilney L.G. Actin filament cables in Drosophila nurse cells are composed of modules that slide passively past one another during dumping. J. Cell Biol. 1997, 138:783-797.
19. Hatan M., Shinder V., Israeli D., Schnorrer F., Volk T. The Drosophila blood brain barrier is maintained by GPCR-dependent dynamic actin structures. J. Cell Biol. 2011, 192:307-319.
20. Hird S. Cortical actin movements during the first cell cycle of the Caenorhabditis elegans embryo. J. Cell Sci. 1996, 109:525-533.
21. Hudson A.M., Cooley L. Understanding the function of actin-binding proteins through genetic analysis of Drosophila oogenesis. Annu. Rev. Genet. 2002, 36:455-488.
22. Huelsmann S., Ylanne J., Brown N.H. Filopodia-like actin cables position nuclei in association with perinuclear actin in Drosophila nurse cells. Dev. Cell 2013, 26:604-615.
23. Johnson H.W., Schell M.J. Neuronal IP3 3-kinase is an F-actin-bundling protein: role in dendritic targeting and regulation of spine morphology. Mol. Biol. Cell 2009, 20:5166-5180.
24. Kato K., Chihara T., Hayashi S. Hedgehog and Decapentaplegic instruct polarized growth of cell extensions in the Drosophila trachea. Development 2004, 131:5253-5261.
25. Kovar D.R., Harris E.S., Mahaffy R., Higgs H.N., Pollard T.D. Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 2006, 124:423-435.
26. Lin A.Y., Prochniewicz E., Henderson D.M., Li B., Ervasti J.M., Thomas D.D. Impacts of dystrophin and utrophin domains on actin structural dynamics: implications for therapeutic design. J. Mol. Biol. 2012, 420:87-98.
27. Mahajan-Miklos S., Cooley L. Intercellular cytoplasm transport during Drosophila oogenesis. Dev. Biol. 1994, 165:336-351.
28. Mahajan-Miklos S., Cooley L. The villin-like protein encoded by the Drosophila quail gene is required for actin bundle assembly during oogenesis. Cell 1994, 78:291-301.
29. McDonald D., Carrero G., Andrin C., de Vries G., Hendzel M.J. Nucleoplasmic beta-actin exists in a dynamic equilibrium between low-mobility polymeric species and rapidly diffusing populations. J. Cell Biol. 2006, 172:541-552.
30. McGuire S.E., Le P.T., Osborn A.J., Matsumoto K., Davis R.L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003, 302:1765-1768.
31. McGuire S.E., Mao Z., Davis R.L. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci. STKE: Signal Trans. Knowl. Environ. 2004, 2004:pl6.
32. Peralta X.G., Toyama Y., Hutson M.S., Montague R., Venakides S., Kiehart D.P., Edwards G.S. Upregulation of forces and morphogenic asymmetries in dorsal closure during Drosophila development. Biophys. J. 2007, 92:2583-2596.
33. Phng L.K., Stanchi F., Gerhardt H. Filopodia are dispensable for endothelial tip cell guidance. Development 2013, 140:4031-4040.
34. Prochniewicz E., Henderson D., Ervasti J.M., Thomas D.D. Dystrophin and utrophin have distinct effects on the structural dynamics of actin. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7822-7827.
35. Rauzi M., Lenne P.F., Lecuit T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 2010, 468:1110-1114.
36. Riedl J., Crevenna A.H., Kessenbrock K., Yu J.H., Neukirchen D., Bista M., Bradke F., Jenne D., Holak T.A., Werb Z., Sixt M., Wedlich-Soldner R. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 2008, 5:605-607.
37. Riedl J., Flynn K.C., Raducanu A., Gartner F., Beck G., Bosl M., Bradke F., Massberg S., Aszodi A., Sixt M., Wedlich-Soldner R. Lifeact mice for studying F-actin dynamics. Nat. Methods 2010, 7:168-169.
38. Roper K., Mao Y., Brown N.H. Contribution of sequence variation in Drosophila actins to their incorporation into actin-based structures in vivo. J. Cell Sci. 2005, 118:3937-3948.
39. Rorth P. Gal4 in the Drosophila female germline. Mech. Dev. 1998, 78:113-118.
40. Saengsawang W., Taylor K.L., Lumbard D.C., Mitok K., Price A., Pietila L., Gomez T.M., Dent E.W. CIP4 coordinates with phospholipids and actin-associated proteins to localize to the protruding edge and produce actin ribs and veils. J. Cell Sci. 2013, 126:2411-2423.
41. Scheer U., Hinssen H., Franke W.W., Jockusch B.M. Microinjection of actin-binding proteins and actin antibodies demonstrates involvement of nuclear actin in transcription of lampbrush chromosomes. Cell 1984, 39:111-122.
42. Skora A.D., Spradling A.C. Epigenetic stability increases extensively during Drosophila follicle stem cell differentiation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7389-7394.
43. Spracklen A.J., Kelpsch D.J., Chen X., Spracklen C.N., Tootle T.L. Prostaglandins temporally regulate cytoplasmic actin bundle formation during Drosophila oogenesis. Mol. Biol. Cell 2014, 25:397-411.
44. Spradling A.C. Developmental genetics of oogenesis. The Development of Drosophila Melanogaster 1993, 1-70. Cold Spring Harbor Laboratory Press, Plainview, NY. B. Martinez-Arias (Ed.).
45. Telley I.A., Gaspar I., Ephrussi A., Surrey T. Aster migration determines the length scale of nuclear separation in the Drosophila syncytial embryo. J. Cell Biol. 2012, 197:887-895.
46. Tootle T.L., Spradling A.C. Drosophila Pxt: a cyclooxygenase-like facilitator of follicle maturation. Development 2008, 135:839-847.
47. Toyama Y., Peralta X.G., Wells A.R., Kiehart D.P., Edwards G.S. Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 2008, 321:1683-1686.
48. van der Honing H.S., van Bezouwen L.S., Emons A.M., Ketelaar T. High expression of Lifeact in Arabidopsis thaliana reduces dynamic reorganization of actin filaments but does not affect plant development. Cytoskeleton 2011, 68:578-587.
49. Vidali L., Rounds C.M., Hepler P.K., Bezanilla M. Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PloS One 2009, 4:e5744.
50. Visa N., Percipalle P. Nuclear functions of actin. Cold Spring Harb. Perspect. Biol. 2010, 2:a000620.
51. Weil T.T., Xanthakis D., Parton R., Dobbie I., Rabouille C., Gavis E.R., Davis I. Distinguishing direct from indirect roles for bicoid mRNA localization factors. Development 2010, 137:169-176.
52. Westerfield M. The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio) 2000, University of Oregon Press, Eugene, OR.
53. Wheatley S., Kulkarni S., Karess R. Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 1995, 121:1937-1946.
54. Winder S.J., Hemmings L., Maciver S.K., Bolton S.J., Tinsley J.M., Davies K.E., Critchley D.R., Kendrick-Jones J. Utrophin actin binding domain: analysis of actin binding and cellular targeting. J. Cell Sci. 1995, 108:63-71.
55. Wu J.Q., Pollard T.D. Counting cytokinesis proteins globally and locally in fission yeast. Science 2005, 310:310-314.
56. Wuhr M., Obholzer N.D., Megason S.G., Detrich H.W., Mitchison T.J. Live imaging of the cytoskeleton in early cleavage-stage zebrafish embryos. Methods Cell Biol. 2011, 101:1-18.
57. Xu H., Ye D., Behra M., Burgess S., Chen S., Lin F. Gbeta1 controls collective cell migration by regulating the protrusive activity of leader cells in the posterior lateral line primordium. Dev. Biol. 2014, 385:316-327.
58. Yi J., Wu X.S., Crites T., Hammer J.A. Actin retrograde flow and actomyosin II arc contraction drive receptor cluster dynamics at the immunological synapse in Jurkat T cells. Mol. Biol. Cell 2012, 23:834-852.
59. Zanet J., Jayo A., Plaza S., Millard T., Parsons M., Stramer B. Fascin promotes filopodia formation independent of its role in actin bundling. J. Cell Biol. 2012, 197:477-486.
60. Zanet J., Stramer B., Millard T., Martin P., Payre F., Plaza S. Fascin is required for blood cell migration during Drosophila embryogenesis. Development 2009, 136:2557-2565.