A functional link between localized Oskar, dynamic microtubules, and endocytosis

Developmental Biology

Volumn 367, Issue 1, 2012, Pages 66-77

  Sanghavi, Paulomi ^a   Lu, Sumin ^a   Gonsalvez, Graydon B ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Actin anchoring; Cell polarity; Kinesin; RNA localization

Indexed keywords

BINDING PROTEIN; END BINDING 1 PROTEIN; KINESIN HEAVY CHAIN PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; OSKAR PROTEIN; PROTEIN CLIP 190; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL POLARITY; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; GENE LOCATION; MICROTUBULE; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

EID: 84861706622     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.04.024     Document Type: Article

References (67)

1. Akhmanova A., Steinmetz M.O. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 2008, 9:309-322.
2. Applewhite D.A., Grode K.D., Keller D., Zadeh A.D., Slep K.C., Rogers S.L. The spectraplakin short stop is an actin-microtubule cross-linker that contributes to organization of the microtubule network. Mol. Biol. Cell 2010, 21:1714-1724.
3. Arnal I., Heichette C., Diamantopoulos G.S., Chretien D. CLIP-170/tubulin-curved oligomers coassemble at microtubule ends and promote rescues. Curr. Biol. 2004, 14:2086-2095.
4. Bacallao R., Antony C., Dotti C., Karsenti E., Stelzer E.H., Simons K. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J. Cell Biol. 1989, 109:2817-2832.
5. Bieling P., Kandels-Lewis S., Telley I.A., van Dijk J., Janke C., Surrey T. CLIP-170 tracks growing microtubule ends by dynamically recognizing composite EB1/tubulin-binding sites. J. Cell Biol. 2008, 183:1223-1233.
6. Bre M.H., Pepperkok R., Hill A.M., Levilliers N., Ansorge W., Stelzer E.H., Karsenti E. Regulation of microtubule dynamics and nucleation during polarization in MDCK II cells. J. Cell Biol. 1990, 111:3013-3021.
7. Brendza R.P., Serbus L.R., Duffy J.B., Saxton W.M. A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 2000, 289:2120-2122.
8. Buey R.M., Mohan R., Leslie K., Walzthoeni T., Missimer J.H., Menzel A., Bjelic S., Bargsten K., Grigoriev I., Smal I., Meijering E., Aebersold R., Akhmanova A., Steinmetz M.O. Insights into EB1 structure and the role of its C-terminal domain for discriminating microtubule tips from the lattice. Mol. Biol. Cell 2011, 22:2912-2923.
9. Cha B.J., Serbus L.R., Koppetsch B.S., Theurkauf W.E. Kinesin I-dependent cortical exclusion restricts pole plasm to the oocyte posterior. Nat. Cell Biol. 2002, 4:592-598.
10. Clark I., Giniger E., Ruohola-Baker H., Jan L.Y., Jan Y.N. Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr. Biol. 1994, 4:289-300.
11. Clark I.E., Jan L.Y., Jan Y.N. Reciprocal localization of nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 1997, 124:461-470.
12. Cochran J.C., Sindelar C.V., Mulko N.K., Collins K.A., Kong S.E., Hawley R.S., Kull F.J. ATPase cycle of the nonmotile kinesin NOD allows microtubule end tracking and drives chromosome movement. Cell 2009, 136:110-122.
13. Cui W., Sproul L.R., Gustafson S.M., Matthies H.J., Gilbert S.P., Hawley R.S. Drosophila Nod protein binds preferentially to the plus ends of microtubules and promotes microtubule polymerization in vitro. Mol. Biol. Cell 2005, 16:5400-5409.
14. Dahlgaard K., Raposo A.A., Niccoli T., St Johnston D. Capu and Spire assemble a cytoplasmic actin mesh that maintains microtubule organization in the Drosophila oocyte. Dev. Cell 2007, 13:539-553.
15. Dixit R., Barnett B., Lazarus J.E., Tokito M., Goldman Y.E., Holzbaur E.L. Microtubule plus-end tracking by CLIP-170 requires EB1. Proc. Natl. Acad. Sci. USA 2009, 106:492-497.
16. Doerflinger H., Benton R., Shulman J.M., Johnston D. The role of PAR-1 in regulating the polarised microtubule cytoskeleton in the Drosophila follicular epithelium. Development 2003, 130:3965-3975.
17. Doerflinger H., Benton R., Torres I.L., Zwart M.F., Johnston D. Drosophila anterior-posterior polarity requires actin-dependent PAR-1 recruitment to the oocyte posterior. Curr. Biol. 2006, 16:1090-1095.
18. Duncan J.E., Warrior R. The cytoplasmic dynein and kinesin motors have interdependent roles in patterning the Drosophila oocyte. Curr. Biol. 2002, 12:1982-1991.
19. Ephrussi A., Dickinson L.K., Lehmann R. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 1991, 66:37-50.
20. Galjart N. CLIPs and CLASPs and cellular dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6:487-498.
21. Galjart N. Plus-end-tracking proteins and their interactions at microtubule ends. Curr. Biol. 2010, 20:R528-537.
22. Goldstein B., Macara I.G. The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 2007, 13:609-622.
23. Gonsalvez G.B., Rajendra T.K., Wen Y., Praveen K., Matera A.G. Sm proteins specify germ cell fate by facilitating oskar mRNA localization. Development 2010, 137:2341-2351.
24. Hirokawa N., Noda Y., Tanaka Y., Niwa S. Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 2009, 10:682-696.
25. Honnappa S., Gouveia S.M., Weisbrich A., Damberger F.F., Bhavesh N.S., Jawhari H., Grigoriev I., van Rijssel F.J., Buey R.M., Lawera A., Jelesarov I., Winkler F.K., Wuthrich K., Akhmanova A., Steinmetz M.O. An EB1-binding motif acts as a microtubule tip localization signal. Cell 2009, 138:366-376.
26. Jenny A., Hachet O., Zavorszky P., Cyrklaff A., Weston M.D., Johnston D.S., Erdelyi M., Ephrussi A. A translation-independent role of oskar RNA in early Drosophila oogenesis. Development 2006, 133:2827-2833.
27. Jiang K., Akhmanova A. Microtubule tip-interacting proteins: a view from both ends. Curr. Opin. Cell Biol. 2010, 23:94-101.
28. Kardon J.R., Vale R.D. Regulators of the cytoplasmic dynein motor. Nat. Rev. Mol. Cell Biol. 2009, 10:854-865.
29. Kim-Ha J., Kerr K., Macdonald P.M. Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell 1995, 81:403-412.
30. Kim-Ha J., Smith J.L., Macdonald P.M. oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 1991, 66:23-35.
31. Komarova Y., De Groot C.O., Grigoriev I., Gouveia S.M., Munteanu E.L., Schober J.M., Honnappa S., Buey R.M., Hoogenraad C.C., Dogterom M., Borisy G.G., Steinmetz M.O., Akhmanova A. Mammalian end binding proteins control persistent microtubule growth. J. Cell Biol. 2009, 184:691-706.
32. Komarova Y.A., Akhmanova A.S., Kojima S., Galjart N., Borisy G.G. Cytoplasmic linker proteins promote microtubule rescue in vivo. J. Cell Biol. 2002, 159:589-599.
33. Krauss J., Lopez de Quinto S., Nusslein-Volhard C., Ephrussi A. Myosin-V regulates oskar mRNA localization in the Drosophila oocyte. Curr. Biol. 2009, 19:1058-1063.
34. Lantz V.A., Miller K.G. A class VI unconventional myosin is associated with a homologue of a microtubule-binding protein, cytoplasmic linker protein-170, in neurons and at the posterior pole of Drosophila embryos. J. Cell Biol. 1998, 140:897-910.
35. Lewkowicz E., Herit F., Le Clainche C., Bourdoncle P., Perez F., Niedergang F. The microtubule-binding protein CLIP-170 coordinates mDia1 and actin reorganization during CR3-mediated phagocytosis. J. Cell Biol. 2008, 183:1287-1298.
36. Ligon L.A., Shelly S.S., Tokito M., Holzbaur E.L. The microtubule plus-end proteins EB1 and dynactin have differential effects on microtubule polymerization. Mol. Biol. Cell 2003, 14:1405-1417.
37. Loiseau P., Davies T., Williams L.S., Mishima M., Palacios I.M. Drosophila PAT1 is required for Kinesin-1 to transport cargo and to maximize its motility. Development 2010, 137:2763-2772.
38. Lomakin A.J., Kraikivski P., Semenova I., Ikeda K., Zaliapin I., Tirnauer J.S., Akhmanova A., Rodionov V. Stimulation of the CLIP-170-dependent capture of membrane organelles by microtubules through fine tuning of microtubule assembly dynamics. Mol. Biol. Cell 2011, 22:4029-4037.
39. Lomakin A.J., Semenova I., Zaliapin I., Kraikivski P., Nadezhdina E., Slepchenko B.M., Akhmanova A., Rodionov V. CLIP-170-dependent capture of membrane organelles by microtubules initiates minus-end directed transport. Dev. Cell 2009, 17:323-333.
40. Luders J., Stearns T. Microtubule-organizing centres: a re-evaluation. Nat. Rev. Mol. Cell Biol. 2007, 8:161-167.
41. Martin K.C., Ephrussi A. mRNA localization: gene expression in the spatial dimension. Cell 2009, 136:719-730.
42. Martin S.G., McDonald W.H., Yates J.R., Chang F. Tea4p links microtubule plus ends with the formin for3p in the establishment of cell polarity. Dev. Cell 2005, 8:479-491.
43. Matov A., Applegate K., Kumar P., Thoma C., Krek W., Danuser G., Wittmann T. Analysis of microtubule dynamic instability using a plus-end growth marker. Nat. Meth. 2010, 7:761-768.
44. Maurer S.P., Bieling P., Cope J., Hoenger A., Surrey T. GTP gamma microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs). Proc. Natl. Acad. Sci. USA 2011, 108:3988-3993.
45. Megraw T.L., Li K., Kao L.R., Kaufman T.C. The centrosomin protein is required for centrosome assembly and function during cleavage in Drosophila. Development 1999, 126:2829-2839.
46. Micklem D.R., Adams J., Grunert S., Johnston D. Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J. 2000, 19:1366-1377.
47. Palacios I.M., Johnston D. Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development 2002, 129:5473-5485.
48. Parton R.M., Hamilton R.S., Ball G., Yang L., Cullen C.F., Lu W., Ohkura H., Davis I. A PAR-1-dependent orientation gradient of dynamic microtubules directs posterior cargo transport in the Drosophila oocyte. J. Cell Biol. 2011, 194:121-135.
49. Pierre P., Scheel J., Rickard J.E., Kreis T.E. CLIP-170 links endocytic vesicles to microtubules. Cell 1992, 70:887-900.
50. Riechmann V., Ephrussi A. Axis formation during Drosophila oogenesis. Curr. Opin. Genet. Dev. 2001, 11:374-383.
51. Rogers S.L., Rogers G.C., Sharp D.J., Vale R.D. Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol. 2002, 158:873-884.
52. Shannon K.B., Canman J.C., Ben Moree C., Tirnauer J.S., Salmon E.D. Taxol-stabilized microtubules can position the cytokinetic furrow in mammalian cells. Mol. Biol. Cell 2005, 16:4423-4436.
53. Shulman J.M., Benton R., Johnston D. The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 2000, 101:377-388.
54. Slep K.C. Structural and mechanistic insights into microtubule end-binding proteins. Curr. Opin. Cell Biol. 2010, 22:88-95.
55. Snee M.J., Macdonald P.M. Live imaging of nuage and polar granules: evidence against a precursor-product relationship and a novel role for Oskar in stabilization of polar granule components. J. Cell Sci. 2004, 117:2109-2120.
56. St Johnston D. Moving messages: the intracellular localization of mRNAs. Nat. Rev. Mol. Cell Biol. 2005, 6:363-375.
57. St Johnston D., Beuchle D., Nusslein-Volhard C. Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 1991, 66:51-63.
58. Tanaka T., Nakamura A. The endocytic pathway acts downstream of Oskar in Drosophila germ plasm assembly. Development 2008, 135:1107-1117.
59. Terada Y., Uetake Y., Kuriyama R. Interaction of Aurora-A and centrosomin at the microtubule-nucleating site in Drosophila and mammalian cells. J. Cell Biol. 2003, 162:757-763.
60. Tomancak P., Piano F., Riechmann V., Gunsalus K.C., Kemphues K.J., Ephrussi A. A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic-axis formation. Nat. Cell Biol. 2000, 2:458-460.
61. van Eeden F., Johnston D. The polarisation of the anterior-posterior and dorsal-ventral axes during Drosophila oogenesis. Curr. Opin. Genet. Dev. 1999, 9:396-404.
62. van Eeden F.J., Palacios I.M., Petronczki M., Weston M.J., Johnston D. Barentsz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole. J. Cell Biol. 2001, 154:511-523.
63. Vanzo N., Oprins A., Xanthakis D., Ephrussi A., Rabouille C. Stimulation of endocytosis and actin dynamics by Oskar polarizes the Drosophila oocyte. Dev. Cell 2007, 12:543-555.
64. Vanzo N.F., Ephrussi A. Oskar anchoring restricts pole plasm formation to the posterior of the Drosophila oocyte. Development 2002, 129:3705-3714.
65. Wiese C., Zheng Y. Microtubule nucleation: gamma-tubulin and beyond. J. Cell Sci. 2006, 119:4143-4153.
66. Zimyanin V., Lowe N., St Johnston D. An oskar-dependent positive feedback loop maintains the polarity of the Drosophila oocyte. Curr. Biol. 2007, 17:353-359.
67. Zimyanin V.L., Belaya K., Pecreaux J., Gilchrist M.J., Clark A., Davis I., St Johnston D. In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 2008, 134:843-853.