Par-1 controls myosin-II activity through myosin phosphatase to regulate border cell migration

Current Biology

Volumn 22, Issue 5, 2012, Pages 363-372

  Majumder, Pralay ^a   Aranjuez, George ^a,b   Amick, Joseph ^a   McDonald, Jocelyn A ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; GLYCOGEN SYNTHASE KINASE 3; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; PAR 1 PROTEIN, DROSOPHILA; PAR-1 PROTEIN, DROSOPHILA; SIGNAL PEPTIDE;

ANIMAL; ARTICLE; CELL MOTION; CELL POLARITY; CYTOSKELETON; DROSOPHILA; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ACTOMYOSIN; ANIMALS; CELL MOVEMENT; CELL POLARITY; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; GLYCOGEN SYNTHASE KINASE 3; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MYOSIN LIGHT CHAINS; MYOSIN TYPE II; MYOSIN-LIGHT-CHAIN PHOSPHATASE; PHOSPHORYLATION;

EID: 84858001709     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2012.01.037     Document Type: Article

References (45)

1. P. Friedl, and D. Gilmour Collective cell migration in morphogenesis, regeneration and cancer Nat. Rev. Mol. Cell Biol. 10 2009 445 457
2. M. Yilmaz, and G. Christofori Mechanisms of motility in metastasizing cells Mol. Cancer Res. 8 2010 629 642
3. D.J. Montell Border-cell migration: the race is on Nat. Rev. Mol. Cell Biol. 4 2003 13 24
4. L. Zhang, J. Luo, P. Wan, J. Wu, F. Laski, and J. Chen Regulation of cofilin phosphorylation and asymmetry in collective cell migration during morphogenesis Development 138 2011 455 464
5. X. Wang, L. He, Y.I. Wu, K.M. Hahn, and D.J. Montell Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo Nat. Cell Biol. 12 2010 591 597
6. A. Bianco, M. Poukkula, A. Cliffe, J. Mathieu, C.M. Luque, T.A. Fulga, and P. Rørth Two distinct modes of guidance signalling during collective migration of border cells Nature 448 2007 362 365
7. M. Prasad, and D.J. Montell Cellular and molecular mechanisms of border cell migration analyzed using time-lapse live-cell imaging Dev. Cell 12 2007 997 1005
8. J.A. McDonald, A. Khodyakova, G. Aranjuez, C. Dudley, and D.J. Montell PAR-1 kinase regulates epithelial detachment and directional protrusion of migrating border cells Curr. Biol. 18 2008 1659 1667
9. D. Matenia, and E.M. Mandelkow The tau of MARK: a polarized view of the cytoskeleton Trends Biochem. Sci. 34 2009 332 342
10. E.M. Pinheiro, and D.J. Montell Requirement for Par-6 and Bazooka in Drosophila border cell migration Development 131 2004 5243 5251
11. M. Vicente-Manzanares, X. Ma, R.S. Adelstein, and A.R. Horwitz Non-muscle myosin II takes centre stage in cell adhesion and migration Nat. Rev. Mol. Cell Biol. 10 2009 778 790
12. N. Gorfinkiel, and G.B. Blanchard Dynamics of actomyosin contractile activity during epithelial morphogenesis Curr. Opin. Cell Biol 23 2011 531 539
13. K.A. Edwards, and D.P. Kiehart Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis Development 122 1996 1499 1511
14. I. Tan, and T. Leung Myosin light chain kinases: division of work in cell migration Cell Adh Migr 3 2009 256 258
15. C.G. Winter, B. Wang, A. Ballew, A. Royou, R. Karess, J.D. Axelrod, and L. Luo Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton Cell 105 2001 81 91
16. S.O. Dean, and J.A. Spudich Rho kinase's role in myosin recruitment to the equatorial cortex of mitotic Drosophila S2 cells is for myosin regulatory light chain phosphorylation PLoS ONE 1 2006 e131
17. P. Jordan, and R. Karess Myosin light chain-activating phosphorylation sites are required for oogenesis in Drosophila J. Cell Biol. 139 1997 1805 1819
18. Y. Wang, and V. Riechmann The role of the actomyosin cytoskeleton in coordination of tissue growth during Drosophila oogenesis Curr. Biol. 17 2007 1349 1355
19. M.E. Grassie, L.D. Moffat, M.P. Walsh, and J.A. Macdonald The myosin phosphatase targeting protein (MYPT) family: A regulated mechanism for achieving substrate specificity of the catalytic subunit of protein phosphatase type 1delta Arch Biochem Biophys 510 2011 147 159
20. T.A. Fulga, and P. Rørth Invasive cell migration is initiated by guided growth of long cellular extensions Nat. Cell Biol. 4 2002 715 719
21. J.D. Franke, R.A. Montague, and D.P. Kiehart Nonmuscle myosin II is required for cell proliferation, cell sheet adhesion and wing hair morphology during wing morphogenesis Dev. Biol. 345 2010 117 132
22. A. Royou, C. Field, J.C. Sisson, W. Sullivan, and R. Karess Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos Mol. Biol. Cell 15 2004 838 850
23. R. Benton, and D. St Johnston Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells Cell 115 2003 691 704
24. M. Amano, M. Ito, K. Kimura, Y. Fukata, K. Chihara, T. Nakano, Y. Matsuura, and K. Kaibuchi Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase) J. Biol. Chem. 271 1996 20246 20249
25. K. Kimura, M. Ito, M. Amano, K. Chihara, Y. Fukata, M. Nakafuku, B. Yamamori, J. Feng, T. Nakano, and K. Okawa Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase) Science 273 1996 245 248
26. D. Bennett, B. Szöor, S. Gross, N. Vereshchagina, and L. Alphey Ectopic expression of inhibitors of protein phosphatase type 1 (PP1) can be used to analyze roles of PP1 in Drosophila development Genetics 164 2003 235 245
27. L. He, X. Wang, H.L. Tang, and D.J. Montell Tissue elongation requires oscillating contractions of a basal actomyosin network Nat. Cell Biol. 12 2010 1133 1142
28. M. Rauzi, P.F. Lenne, and T. Lecuit Planar polarized actomyosin contractile flows control epithelial junction remodelling Nature 468 2010 1110 1114
29. A.C. Martin, M. Kaschube, and E.F. Wieschaus Pulsed contractions of an actin-myosin network drive apical constriction Nature 457 2009 495 499
30. A. Lee, and J.E. Treisman Excessive Myosin activity in mbs mutants causes photoreceptor movement out of the Drosophila eye disc epithelium Mol. Biol. Cell 15 2004 3285 3295
31. A. Zagórska, M. Deak, D.G. Campbell, S. Banerjee, M. Hirano, S. Aizawa, A.R. Prescott, and D.R. Alessi New roles for the LKB1-NUAK pathway in controlling myosin phosphatase complexes and cell adhesion Sci. Signal. 3 2010 ra25
32. S. Wilkinson, H.F. Paterson, and C.J. Marshall Cdc42-MRCK and Rho-ROCK signalling cooperate in myosin phosphorylation and cell invasion Nat. Cell Biol. 7 2005 255 261
33. N. Vereshchagina, D. Bennett, B. Szöor, J. Kirchner, S. Gross, E. Vissi, H. White-Cooper, and L. Alphey The essential role of PP1beta in Drosophila is to regulate nonmuscle myosin Mol. Biol. Cell 15 2004 4395 4405
34. P.T. Yam, C.A. Wilson, L. Ji, B. Hebert, E.L. Barnhart, N.A. Dye, P.W. Wiseman, G. Danuser, and J.A. Theriot Actin-myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility J. Cell Biol. 178 2007 1207 1221
35. A.B. Verkhovsky, T.M. Svitkina, and G.G. Borisy Self-polarization and directional motility of cytoplasm Curr. Biol. 9 1999 11 20
36. M. Vicente-Manzanares, K. Newell-Litwa, A.I. Bachir, L.A. Whitmore, and A.R. Horwitz Myosin IIA/IIB restrict adhesive and protrusive signaling to generate front-back polarity in migrating cells J. Cell Biol. 193 2011 381 396
37. J.B. Hurov, J.L. Watkins, and H. Piwnica-Worms Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity Curr. Biol. 14 2004 736 741
38. E. Sahai, and C.J. Marshall ROCK and Dia have opposing effects on adherens junctions downstream of Rho Nat. Cell Biol. 4 2002 408 415
39. M. Smutny, H.L. Cox, J.M. Leerberg, E.M. Kovacs, M.A. Conti, C. Ferguson, N.A. Hamilton, R.G. Parton, R.S. Adelstein, and A.S. Yap Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens Nat. Cell Biol. 12 2010 696 702
40. M. Vicente-Manzanares, J. Zareno, L. Whitmore, C.K. Choi, and A.F. Horwitz Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells J. Cell Biol. 176 2007 573 580
41. G. Giannone, B.J. Dubin-Thaler, O. Rossier, Y. Cai, O. Chaga, G. Jiang, W. Beaver, H.G. Döbereiner, Y. Freund, G. Borisy, and M.P. Sheetz Lamellipodial actin mechanically links myosin activity with adhesion-site formation Cell 128 2007 561 575
42. D. Neubueser, and D.R. Hipfner Overlapping roles of Drosophila Drak and Rok kinases in epithelial tissue morphogenesis Mol. Biol. Cell 21 2010 2869 2879
43. C. Gally, F. Wissler, H. Zahreddine, S. Quintin, F. Landmann, and M. Labouesse Myosin II regulation during C. elegans embryonic elongation: LET-502/ROCK, MRCK-1 and PAK-1, three kinases with different roles Development 136 2009 3109 3119
44. C. Hidalgo-Carcedo, S. Hooper, S.I. Chaudhry, P. Williamson, K. Harrington, B. Leitinger, and E. Sahai Collective cell migration requires suppression of actomyosin at cell-cell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6 Nat. Cell Biol. 13 2011 49 58
45. R. Benton, I.M. Palacios, and D. St Johnston Drosophila 14-3-3/PAR-5 is an essential mediator of PAR-1 function in axis formation Dev. Cell 3 2002 659 671