Genetic evidence for concerted control of actin dynamics in cytokinesis, endocytic traffic, and cell motility by coronin and Aip1

Cytoskeleton

Volumn 67, Issue 7, 2010, Pages 442-455

  Ishikawa Ankerhold, Hellen C ^a   Gerisch, Günther ^a   Muller Taubenberger, Annette ^b  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Actin; Aip1; Cell motility; Chemotaxis; Coronin; Cytokinesis; Dictyostelium; Phagocytosis

Indexed keywords

ACTIN INTERACTING PROTEIN 1; CHEMOATTRACTANT; F ACTIN; KHELLIN; LATRUNCULIN A; PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; CELL DIVISION; CELL MIGRATION; CELL MOTILITY; CELL MUTANT; CELL POLARITY; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINESIS; CYTOSKELETON; DICTYOSTELIUM DISCOIDEUM; ENDOCYTOSIS; NONHUMAN; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE;

4-BUTYROLACTONE; ACTIN CYTOSKELETON; ACTIN DEPOLYMERIZING FACTORS; ACTINS; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL MOVEMENT; CELL POLARITY; CELL SHAPE; CHEMOTAXIS; CYTOKINESIS; DICTYOSTELIUM; ENDOCYTOSIS; MICROFILAMENT PROTEINS; MITOSIS; MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT; THIAZOLIDINES;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM;

EID: 77955893542     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.20456     Document Type: Article

References (71)

1. Aizawa H, Fukui Y, Yahara I. 1997. Live dynamics of Dictyostelium cofilin suggests a role in remodeling actin latticework into bundles. J Cell Sci 110: 2333-2344.
2. Aizawa H, Katadae M, Maruya M, Sameshima M, Murakami-Murofushi K, Yahara I. 1999. Hyperosmotic stress-induced reorganization of actin bundles in Dictyostelium cells over-expressing cofilin. Genes Cells 4:311-324.
3. Appleton BA, Wu P, Wiesmann C. 2006. The crystal structure of murine coronin-1: A regulator of actin cytoskeletal dynamics in lymphocytes. Structure 14:87-96.
4. Bertholdt G, Stadler J, Bozzaro S, Fichtner B, Gerisch G. 1985. Carbohydrate and other epitopes of the contact site A glycoprotein of Dictyostelium discoideum as characterized by monoclonal antibodies. Cell Differ 16: 187-202.
5. Biron D, Libros P, Sagi D, Mirelman D, Moses E. 2001. Asexual reproduction: 'Midwives' assist dividing amoebae. Nature 410:430.
6. Bretschneider T, Diez S, Anderson K, Heuser J, Clarke M, Müller-Taubenberger A, Köhler J, Gerisch G. 2004. Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. Curr Biol 14: 1-10.
7. Bretschneider T, Anderson K, Ecke M, Müller-Taubenberger A, Schroth-Diez B, Ishikawa-Ankerhold HC, Gerisch G. 2009. The three-dimensional dynamics of actin waves, a model of cytoskeletal self-organization. Biophys J 96:2888-2900.
8. Brieher WM, Kueh HY, Ballif BA, Mitchison TJ. 2006. Rapid actin monomer-insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. J Cell Biol 175:315-324.
9. Cai L, Holoweckyj N, Schaller MD, Bear JE. 2005. Phosphorylation of coronin 1B by protein kinase C regulates interaction with Arp2/3 and cell motility. J Biol Chem 280(36):31913-31923.
10. Cai L, Marshall TW, Uetrecht AC, Schafer DA, Bear JE. 2007. Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell 128:915-929.
11. Cai L, Makhov AM, Schafer DA, Bear JE. 2008. Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia. Cell 134:828-842.
12. Cano ML, Cassimeris L, Joyce M, Zigmond SH. 1992. Characterization of tetramethylrhodaminyl-phalloidin binding to cellular F-actin. Cell Motil Cytoskeleton 21:147-158.
13. Clark MG, Teply J, Haarer BK, Viggiano SC, Sept D, Amberg DC. 2006. A genetic dissection of Aip1p's interactions leads to a model for Aip1p-cofilin cooperative activities. Mol Biol Cell 17:1971-1984.
14. Clarke M, Maddera L. 2006. Phagocyte meets prey: Uptake, internalization, and killing of bacteria by Dictyostelium amoebae. Eur J Cell Biol 85: 1001-1010.
15. Clarke M, Müller-Taubenberger A, Anderson KI, Engel U, Gerisch G. 2006. Mechanically induced actin-mediated rocketing of phagosomes. Mol Biol Cell 17:4866-4875.
16. Claviez M, Brink M, Gerisch G. 1986. Cytoskeletons from a mutant of Dictyostelium discoideum with flattened cells. J Cell Sci 86:69-82.
17. de Hostos EL. 1999. The coronin family of actin-associated proteins. Trends Cell Biol 9:345-350.
18. de Hostos EL, Bradtke B, Lottspeich F, Guggenheim R, Gerisch G. 1991. Coronin, an actin binding protein of Dictyostelium discoideum localized to cell surface projections, has sequence similarities to G protein beta subunits. EMBO J 10:4097-4104.
19. de Hostos EL, Rehfuess C, Bradtke B, Waddell DR, Albrecht R, Murphy J, Gerisch G. 1993. Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. J Cell Biol 120:163-173.
20. De Lozanne A, Spudich JA. 1987. Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236: 1086-1091.
21. Defacque H, Egeberg M, Habermann A, Diakonova M, Roy C, Mangeat P, Voelter W, Marriott G, Pfannstiel J, Faulstich H, et al. 2000. Involvement of ezrin/moesin in de novo actin assembly on phagosomal membranes. EMBO J 19:199-212.
22. Diez S, Gerisch G, Anderson K, Müller-Taubenberger A, Bretschneider T. 2005. Subsecond reorganization of the actin network in cell motility and chemotaxis. Proc Natl Acad Sci USA 102:7601-7606.
23. Etzrodt M, Ishikawa HC, Dalous J, Müller-Taubenberger A, Bretschneider T, Gerisch G. 2006. Time-resolved responses to chemoattractant, characteristic of the front and tail of Dictyostelium cells. FEBS Lett 580:6707-6713.
24. Faix J, Gerisch G, Noegel AA. 1992. Overexpression of the csA cell adhesion molecule under its own cAMP-regulated promoter impairs morphogenesis in Dictyostelium. J Cell Sci 102:203-214.
25. Föger N, Rangell L, Danilenko DM, Chan AC. 2006. Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science 313: 839-842.
26. Gandhi M, Goode BL. 2008. Coronin: The double-edged sword of actin dynamics. Subcell Biochem 48:72-87.
27. Gandhi M, Achard V, Blanchoin L, Goode BL. 2009. Coronin switches roles in actin disassembly depending on the nucleotide state of actin. Mol Cell 34:364-374.
28. Gerisch G, Albrecht R, Heizer C, Hodgkinson S, Maniak M. 1995. Chemoattractant-controlled accumulation of coronin at the leading edge of Dictyostelium cells monitored using a green fluorescent protein-coronin fusion protein. Curr Biol 5:1280-1285.
29. Gerisch G, Bretschneider T, Müller-Taubenberger A, Simmeth E, Ecke M, Diez S, Anderson K. 2004a. Mobile actin clusters and traveling waves in cells recovering from actin depolymerization. Biophys J 87:3493-3503.
30. Gerisch G, Faix J, Köhler J, Müller-Taubenberger A. 2004b. Actin-binding proteins required for reliable chromosome segregation in mitosis. Cell Motil Cytoskeleton 57:18-25.
31. Goode BL, Wong JJ, Butty AC, Peter M, McCormack AL, Yates JR, Drubin DG, Barnes G. 1999. Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast. J Cell Biol 144:83-98.
32. Gräf R, Euteneuer U, Ueda M, Schliwa M. 1998. Isolation of nucleationcompetent centrosomes from Dictyostelium discoideum. Eur J Cell Biol 76: 167-175.
33. Hall AL, Schlein A, Condeelis J. 1988. Relationship of pseudopod extension to chemotactic hormone-induced actin polymerization in amoeboid cells. J Cell Biochem 37:285-299.
34. Haugwitz M, Noegel AA, Karakesisoglou J, Schleicher M. 1994. Dictyostelium amoebae that lack G-actin-sequestering profilins show defects in F-actin content, cytokinesis, and development. Cell 79:303-314.
35. Heinrich D, Youssef S, Schroth-Diez B, Engel U, Aydin D, Blummel J, Spatz JP, Gerisch G. 2008. Actin-cytoskeleton dynamics in non-monotonic cell spreading. Cell Adh Migr 2:58-68.
36. Howard TH, Oresajo CO. 1985. A method for quantifying F-actin in chemotactic peptide activated neutrophils: study of the effect of tBOC peptide. Cell Motil 5:545-557.
37. Humphries CL, Balcer HI, D'Agostino JL, Winsor B, Drubin DG, Barnes G, Andrews BJ, Goode BL. 2002. Direct regulation of Arp2/3 complex activity and function by the actin binding protein coronin. J Cell Biol 159:993-1004.
38. Isik N, Brzostowski JA, Jin T. 2008. An Elmo-like protein associated with myosin II restricts spurious F-actin events to coordinate phagocytosis and chemotaxis. Dev Cell 15:590-602.
39. Jenne N, Rauchenberger R, Hacker U, Kast T, Maniak M. 1998. Targeted gene disruption reveals a role for vacuolin B in the late endocytic pathway and exocytosis. J Cell Sci 111:61-70.
40. Kato A, Kurita S, Hayashi A, Kaji N, Ohashi K, Mizuno K. 2008. Critical roles of actin-interacting protein 1 in cytokinesis and chemotactic migration of mammalian cells. Biochem J 414:261-270.
41. Kimmel AR, Parent CA. 2003. The signal to move: D. discoideum go orienteering. Science 300:1525-1527.
42. Knecht DA, Loomis WF. 1988. Developmental consequences of the lack of myosin heavy chain in Dictyostelium discoideum. Dev Biol 128:178-184.
43. Konzok A, Weber I, Simmeth E, Hacker U, Maniak M, Müller- Taubenberger A. 1999. DAip1, a Dictyostelium homologue of the yeast actin-interacting protein 1, is involved in endocytosis, cytokinesis, and motility. J Cell Biol 146:453-464.
44. Lee E, Shelden EA, Knecht DA. 1998. Formation of F-actin aggregates in cells treated with actin stabilizing drugs. Cell Motil Cytoskeleton 39:122-133.
45. Maniak M, Rauchenberger R, Albrecht R, Murphy J, Gerisch G. 1995. Coronin involved in phagocytosis: Dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag. Cell 83:915-924.
46. Nagasaki A, Uyeda TQ. 2008. Chemotaxis-mediated scission contributes to efficient cytokinesis in Dictyostelium. Cell Motil Cytoskeleton 65:896-903.
47. Nakamura T, Takeuchi K, Muraoka S, Takezoe H, Takahashi N, Mori N. 1999. A neurally enriched coronin-like protein. ClipinC, is a novel candidate for an actin cytoskeleton-cortical membrane-linking protein. J Biol Chem 274:13322-13327.
48. Neujahr R, Heizer C, Gerisch G. 1997. Myosin II-independent processes in mitotic cells of Dictyostelium discoideum: redistribution of the nuclei, rearrangement of the actin system and formation of the cleavage furrow. J Cell Sci 110:123-137.
49. Okada K, Obinata T, Abe H. 1999. XAIP1: A Xenopus homologue of yeast actin interacting protein 1 (AIP1), which induces disassembly of actin filaments cooperatively with ADF/cofilin family proteins. J Cell Sci 112: 1553-1565.
50. Okada K, Blanchoin L, Abe H, Chen H, Pollard TD, Bamburg JR. 2002. Xenopus actin-interacting protein 1 (XAip1) enhances cofilin fragmentation of filaments by capping filament ends. J Biol Chem 277:43011-43016.
51. Okada K, Ravi H, Smith EM, Goode BL. 2006. Aip1 and cofilin promote rapid turnover of yeast actin patches and cables: A coordinated mechanism for severing and capping filaments. Mol Biol Cell 17:2855-2868.
52. Oku T, Itoh S, Ishii R, Suzuki K, Nauseef WM, Toyoshima S, Tsuji T. 2005. Homotypic dimerization of the actin-binding protein p57/coronin-1 mediated by a leucine zipper motif in the C-terminal region. Biochem J 387:325-331.
53. Ono S. 2003. Regulation of actin filament dynamics by actin depolymerizing factor/cofilin and actin-interacting protein 1: New blades for twisted filaments. Biochemistry 42:13363-13370.
54. Ono S, Mohri K, Ono K. 2004. Microscopic evidence that actin-interacting protein 1 actively disassembles actin-depolymerizing factor/Cofilin-bound actin filaments. J Biol Chem 279:14207-14212.
55. Pollard TD, Borisy GG. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-465.
56. Rodal AA, Tetreault JW, Lappalainen P, Drubin DG, Amberg DC. 1999. Aip1p interacts with cofilin to disassemble actin filaments. J Cell Biol 145: 1251-1264.
57. Rodal AA, Sokolova O, Robins DB, Daugherty KM, Hippenmeyer S, Riezman H, Grigorieff N, Goode BL. 2005. Conformational changes in the Arp2/3 complex leading to actin nucleation. Nat Struct Mol Biol 12: 26-31.
58. Rogers SL, Wiedemann U, Stuurman N, Vale RD. 2003. Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J Cell Biol 162:1079-1088.
59. Rohlfs M, Arasada R, Batsios P, Janzen J, Schleicher M. 2007. The Ste20-like kinase SvkA of Dictyostelium discoideum is essential for late stages of cytokinesis. J Cell Sci 120:4345-4354.
60. Shina MC, Ünal C, Eichinger L, Müller-Taubenberger A, Schleicher M, Steinert M, Noegel AA. 2010. A coronin7 homolog with functions in actindriven processes. J Biol Chem 285:9249-9261.
61. Siripala AD, Welch MD. 2007a. SnapShot: Actin regulators I. Cell 128:626.
62. Siripala AD, Welch MD. 2007b. SnapShot: Actin regulators II. Cell 128: 1014.
63. Spoerl Z, Stumpf M, Noegel AA, Hasse A. 2002. Oligomerization. F-actin interaction, and membrane association of the ubiquitous mammalian coronin 3 are mediated by its carboxyl terminus. J Biol Chem 277: 48858-48867.
64. Troll H, Malchow D, Müller-Taubenberger A, Humbel B, Lottspeich F, Ecke M, Gerisch G, Schmid A, Benz R. 1992. Purification, functional characterization, and cDNA sequencing of mitochondrial porin from Dictyostelium discoideum. J Biol Chem 267:21072-21079.
65. Uetrecht AC, Bear JE. 2006. Coronins: the return of the crown. Trends Cell Biol 16:421-426.
66. Voegtli WC, Madrona AY, Wilson DK. 2003. The structure of Aip1p, a WD repeat protein that regulates Cofilin-mediated actin depolymerization. J Biol Chem 278:34373-34379.
67. Wallraff E, Gerisch G. 1991. Screening for Dictyostelium mutants defective in cytoskeletal proteins by colony immunoblotting. Methods Enzymol 196: 334-348.
68. Watts DJ, Ashworth JM. 1970. Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J 119: 171-174.
69. Westphal M, Jungbluth A, Heidecker M, Mühlbauer B, Heizer C, Schwartz JM, Marriott G, Gerisch G. 1997. Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr Biol 7:176-183.
70. Willard SS, Devreotes PN. 2006. Signaling pathways mediating chemotaxis in the social amoeba Dictyostelium discoideum. Eur J Cell Biol 85:897-904.
71. Yan M, Di Ciano-Oliveira C, Grinstein S, Trimble WS. 2007. Coronin function is required for chemotaxis and phagocytosis in human neutrophils. J Immunol 178:5769-5778.