Capping protein is essential for cell migration in vivo and for filopodial morphology and dynamics

Molecular Biology of the Cell

Volumn 25, Issue 14, 2014, Pages 2152-2160

  Sinnar, Shamim A ^a   Antoku, Susumu ^b,c   Saffin, Jean Michel ^a   Cooper, Jon A ^b   Halpain, Shelley ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPPING PROTEIN; F ACTIN; METHENAMINE; PHALLOIDIN; POLYCLONAL ANTIBODY; PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ACTIN; PROTEIN CAPZ;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL MOTILITY; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; ELECTROPORATION; FILOPODIUM; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; MAMMAL CELL; MOUSE; NEOCORTEX; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; U2OS CELL LINE; ANIMAL; CELL MOTION; GENE SILENCING; METABOLISM; PHYSIOLOGY; PSEUDOPODIUM; TUMOR CELL LINE; ULTRASTRUCTURE;

ACTINS; ANIMALS; CAPZ ACTIN CAPPING PROTEIN; CELL LINE, TUMOR; CELL MOVEMENT; CELL SHAPE; GENE KNOCKDOWN TECHNIQUES; MICE; PSEUDOPODIA;

EID: 84904332552     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-12-0749     Document Type: Article

References (42)

1. Applewhite DA, Barzik M, Kojima S, Svitkina TM, Gertler FB, Borisy GG (2007). Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol Biol Cell 18, 2579-2591. (Pubitemid 47025723)
2. Arjonen A, Kaukonen R, Ivaska J (2011). Filopodia and adhesion in cancer cell motility. Cell Adhes Migration 5, 421-430.
3. Bartolini F, Ramalingam N, Gundersen GG (2012). Actin-capping protein promotes microtubule stability by antagonizing the actin activity of mDia1. Mol Biol Cell 23, 4032-4040.
4. Bielas S, Higginbotham H, Koizumi H, Tanaka T, Gleeson JG (2004). Cortical neuronal migration mutants suggest separate but intersecting pathways. Annu Rev Cell Dev Biol 20, 593-618. (Pubitemid 39488651)
5. Brummelkamp TR, Bernards R, Agami R (2002). A system for stable expression of short interfering RNAs in mammalian cells. Science 296, 550-553. (Pubitemid 34408678)
6. Calabrese B, Halpain S (2005). Essential role for the PKC target MARCKS in maintaining dendritic spine morphology. Neuron 48, 77-90. (Pubitemid 41384167)
7. Carlier M-F, Pantaloni D (1997). Control of actin dynamics in cell motility. J Mol Biol 269, 459-467. (Pubitemid 27267859)
8. Davis DA, Wilson MH, Giraud J, Xie Z, Tseng H-C, England C, Herscovitz H, Tsai L-H, Delalle I (2009). Capzb2 interacts with β-tubulin to regulate growth cone morphology and neurite outgrowth. PLoS Biol 7, e1000208.
9. Derivery E, Sousa C, Gautier JJ, Lombard B, Loew D, Gautreau A (2009). The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell 17, 712-723.
10. Edwards M, Liang Y, Kim T, Cooper J (2013). Physiological role of the interaction between CARMIL1 and capping protein. Mol Biol Cell 24, 3047-3055.
11. Faix J, Breitsprecher D, Stradal TEB, Rottner K (2009). Filopodia: complex models for simple rods. Int J Biochem Cell Biol 41, 1656-1664.
12. Faix J, Rottner K (2006). The making of filopodia. Curr Opin Cell Biol 18, 18-25. (Pubitemid 43107603)
13. Gallo G (2013). Mechanisms underlying the initiation and dynamics of neuronal filopodia: from neurite formation to synaptogenesis. Int Rev Cell Mol Biol 301, 95-156.
14. Gupton SL, Anderson KL, Kole TP, Fischer RS, Ponti A, Hitchcock-DeGregori SE, Danuser G, Fowler VM, Wirtz D, Hanein D (2005). Cell migration without a lamellipodium translation of actin dynamics into cell movement mediated by tropomyosin. J Cell Biol 168, 619-631. (Pubitemid 40271027)
15. Gupton SL, Gertler FB (2007). Filopodia: the fingers that do the walking. Sci Signaling 2007, re5.
16. Hotulainen P, Paunola E, Vartiainen MK, Lappalainen P (2005). Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells. Mol Biol Cell 16, 649-664. (Pubitemid 40165562)
17. Hu L, Papoian GA (2010). Mechano-chemical feedbacks regulate actin mesh growth in lamellipodial protrusions. Biophys J 98, 1375-1384.
18. Hug C, Jay PY, Reddy I, McNally JG, Bridgman PC, Elson EL, Cooper JA (1995). Capping protein levels influence actin assembly and cell motility in Dictyostelium. Cell 81, 591-600.
19. Iwasa JH, Mullins RD (2007). Spatial and temporal relationships between actin-filament nucleation, capping, and disassembly. Curr Biol 17, 395-406.
20. Lebrand C, Dent EW, Strasser GA, Lanier LM, Krause M, Svitkina TM, Borisy GG, Gertler FB (2004). Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42, 37-49. (Pubitemid 38456966)
21. Le Clainche C, Carlier M-F (2008). Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev 88, 489-513. (Pubitemid 351520086)
22. Lewis AK, Bridgman C (1992). Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. J Cell Biol 119, 1219-1243.
23. Loisel TP, Boujemaa R, Pantaloni D, Carlier M-F (1999). Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613-616.
24. Mallavarapu A, Mitchison T (1999). Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J Cell Biol 146, 1097-1106. (Pubitemid 29430450)
25. Mattila PK, Lappalainen P (2008). Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9, 446-454. (Pubitemid 351733400)
26. Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, Borisy GG (2004). Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118, 363-373. (Pubitemid 39061116)
27. Mogilner A, Rubinstein B (2005). The physics of filopodial protrusion. Biophys J 89, 782-795. (Pubitemid 41098966)
28. Pollard TD, Borisy GG (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465. (Pubitemid 36263079)
29. Ponti A, Machacek M, Gupton S, Waterman-Storer C, Danuser G (2004). Two distinct actin networks drive the protrusion of migrating cells. Science 305, 1782-1786. (Pubitemid 39249647)
30. 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. (Pubitemid 37174190)
31. Schafer DA, Gill SR, Cooper JA, Heuser JE, Schroer TA (1994). Ultrastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin. J Cell Biol 126, 403-412. (Pubitemid 24226256)
32. Schafer DA, Welch MD, Machesky LM, Bridgman PC, Meyer SM, Cooper JA (1998). Visualization and molecular analysis of actin assembly in living cells. J Cell Biol 143, 1919-1930. (Pubitemid 29022613)
33. Simó S, Jossin Y, Cooper JA (2010). Cullin 5 regulates cortical layering by modulating the speed and duration of Dab1-dependent neuronal migration. J Neurosci 30, 5668-5676.
34. Small J (1981). Organization of actin in the leading edge of cultured cells: influence of osmium tetroxide and dehydration on the ultrastructure of actin meshworks. J Cell Biol 91, 695-705.
35. Suraneni P, Rubinstein B, Unruh JR, Durnin M, Hanein D, Li R (2012). The Arp2/3 complex is required for lamellipodia extension and directional fibroblast cell migration. J Cell Biol 197, 239-251.
36. Svitkina TM, Bulanova EA, Chaga OY, Vignjevic DM, Kojima S, Vasiliev JM, Borisy GG (2003). Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol 160, 409-421. (Pubitemid 36182731)
37. Vignjevic D, Kojima S-i, Aratyn Y, Danciu O, Svitkina T, Borisy GG (2006). Role of fascin in filopodial protrusion. J Cell Biol 174, 863-875. (Pubitemid 44373735)
38. Wear MA, Cooper JA (2004). Capping protein: new insights into mechanism and regulation. Trends Biochem Sci 29, 418-428. (Pubitemid 39061086)
39. Wear MA, Yamashita A, Kim K, Maéda Y, Cooper JA (2003). How capping protein binds the barbed end of the actin filament. Curr Biol 13, 1531-1537. (Pubitemid 37078410)
40. Wu C, Asokan S, Berginski M, Haynes E, Sharpless N, Griffith J, Gomez S, Bear J (2012). Arp2/3 is critical for lamellipodia and response to extracellular matrix cues but is dispensable for chemotaxis. Cell 148, 973-987.
41. Yang C, Czech L, Gerboth S, Kojima S-i, Scita G, Svitkina T (2007). Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol 5, e317.
42. Zhuravlev PI, Papoian GA (2009). Molecular noise of capping protein binding induces macroscopic instability in filopodial dynamics. Proc Natl Acad Sci USA 106, 11570-11575.