The role of filament-packing dynamics in powering amoeboid cell motility

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 14, 2008, Pages 5390-5395

  Miao, Long ^a,d   Vanderlinde, Orion ^a   Liu, Jun ^a   Grant, Richard P ^b,e   Wouterse, Alan ^c   Shimabukuro, Katsuya ^a   Philipse, Albert ^c   Stewart, Murray ^b   Roberts, Thomas M ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c UTRECHT UNIVERSITY   (Netherlands)

^d INSTITUTE OF BIOPHYSICS   (China)

^e UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Leading edge; Major sperm protein; Protrusion

Indexed keywords

MAJOR SPERM PROTEIN; MUTANT PROTEIN; PROTEIN DERIVATIVE;

AMOEBOID CELL; ANIMAL CELL; ARTICLE; CELL; CELL MOTILITY; CYTOSKELETON; DENSITY; DYNAMICS; ENGINEERING; FORCE; GEL; HYPOTHESIS; MALE; MEMBRANE; NEMATODE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; SPERMATOZOON MOTILITY; TOMOGRAPHY;

ANIMALS; ASCARIS SUUM; CYTOSKELETON; HELMINTH PROTEINS; MICROFILAMENTS; MOLECULAR MOTOR PROTEINS; MOVEMENT; MUTANT PROTEINS; TOMOGRAPHY;

EID: 44449167997     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0708416105     Document Type: Article

References (40)

1. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-465.
2. Small JV, Stradal T, Vignal E, Rottner K (2002) The lamellipodium: where motility begins. Trends Cell Biol 12:112-120.
3. Carlier MF, Le Clainche CL, Weisner S, Pantaloni D (2003) Actin-based motility: from molecules to movement. BioEssays 25:336-345.
4. Mogilner A, Oster G (2003) Polymer motors: pushing out the front and pulling up the back. Curr Biol 13:R721-R733.
5. Condeelis J, Singer RH, Segall JE (2005) The great escape: when cancer cells hijack the genes for chemotaxis and motility. Annu Rev Cell Dev Biol 21:695-718.
6. Mogilner A (2006) On the edge: modeling protrusion. Curr Opin Cell Biol 17:1-8.
7. Mogilner A, Oster G (2003) Force generation by actin polymerization II: the elastic ratchet and tethered filaments. Biophys J 84:1591-1605.
8. Roberts TM, Stewart M (2000) Acting like actin: the dynamics of nematode major sperm protein (MSP) cytoskeleton indicate a push-pull mechanism for amoeboid cell motility. J Cell Biol 149:7-12.
9. Theriot J (1996) Worm sperm and advances in cell locomotion. Cell 12:1-4.
10. Mogilner A, Oster G (2003) Cell biology: shrinking gels pull cells. Science 302:1340-1341.
11. Italiano JE, Roberts TM, Stewart M, Fontana CA (1996) Reconstitution in vitro of the motile apparatus from the amoeboid sperm of Ascaris shows that filament assembly and bundling move membranes. Cell 84:105-114.
12. Roberts TM, Salmon E, Stewart M (1998) Hydrostatic pressure shows that lamellipodial motility in Ascaris sperm requires membrane-associated major sperm protein filament nucleation and elongation. J Cell Biol 140:367-375.
13. Medalia O, Weber I, Frangakis AS, Nicastro D, Gerisch G, Baumeister W (2002) Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography Science 298:1209-1213
14. Underwood EE (1970) Quantitative Stereology (Addison-Wesley, New York).
15. Philipse AP (1996) (1996) The random contact equation and its implications for (colloidal) rods in packings, suspensions, and anisotropic powders. Langmuir 12:1127-1133 [Addendum, Langmuir 12:5971.
16. Williams SR, Philipse A (2003) Random packings of spheres and spherocylinders simulated by mechanical contraction. Phys Rev E 67:151301.
17. Philipse A, Wierenga AM (1998) On the density and structure formation in gels and clusters of colloidal rods and fibers. Langmuir 14:49-54.
18. Roney D, Fivel M, Dendievel R (2005) Discrete modeling of entangled materials. Phys Rev Lett 95:108004.
19. Rubinstein M, Colby RH (2003) Polymer Physics (Oxford Univ Press, Oxford, UK).
20. Doi M, Edwards SF (1986) The Theory of Polymer Dynamics (Oxford Univ Press, Oxford, UK).
21. Doi M (1996) Introduction to Polymer Physics (Clarendon Press, Gloucestershire, UK).
22. Bullock TL, McCoy AJ, Kent HM, Roberts TM, Stewart M (1998) Structural basis for amoeboid motility in nematode sperm. Nat Struct Biol 5:184-189.
23. Baker AME, Roberts TM, Stewart M (2002) 2.6 Å resolution crystal structure of helices of the motile major sperm protein (MSP) of Caenorhabditis elegans. J Mol Biol 319:491-499.
24. King KL, Stewart M, Roberts TM, Seavy M (1992) Structure and macromolecular assembly of two isoforms of the major sperm protein (MSP) from amoeboid sperm of the nematode Ascaris suum. J Cell Sci 101:847-857.
25. Plastino J, Sykes C (2005) The actin slingshot. Curr Opin Cell Biol 17:62-66
26. Sepsenwol S, Ris H, Roberts TM (1989) A unique cytoskeleton associated with crawling in the amoeboid sperm of the nematode, Ascaris suum. J Cell Biol 108:55-66.
27. King KL, Stewart M, Roberts TM (1994) Supramolecular assemblies of the Ascaris suum major sperm protein (MSP) associated with amoeboid cell motility. J Cell Sci 107:2941-2949.
28. Xu J, Wirtz D, Pollard TD (1998) Dynamic cross-linking by alpha-actinin determines the mechanical properties of actin filament networks. J Biol Chem 273:9570-9576.
29. Tseng Y, An KM, Euse O, Wirtz D (2004) The bimodal role of filamin in controlling the architecture and mechanics of F-actin networks. J Biol Chem 279:1819-1826.
30. Svitkina TM, Borisy GG (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145:1009-1026.
31. Borisy GG, Svitkina TM (2000) Actin machinery: pushing the envelope. Curr Opin Cell Biol 12:104-112.
32. Cameron LA, Svitkina TM, Vignjevic D, Theriot JA, Borisy GG (2001) Dendritic organization of actin comet tails. Curr Biol 11:130-135.
33. Le Clainche C, Pantaloni D, Carlier MF (2003) ATP hydrolysis on actin-related protein 2/3 complex causes debranching of dendritic actin arrays. Proc Natl Acad Sci USA 100:6337-6342.
34. Di Nardo A, Cicchetti G, Falet H, Hartwig JH, Stossel TP, Kwiatkowski DJ (2005) Arp2/3 complex-deficient mouse fibroblasts are viable and have normal leading-edge actin structure and function. Proc Natl Acad Sci USA 102:16263-16268.
35. Orlova A, Egelman EH (1993) A conformational change in the actin subunit can change the flexibility of the actin filament. J Mol Biol 232:334-341.
36. De La Cruz EM, Mandinova A, Steinmetz MO, Stoffler D, Aebi U, Pollard TD (2000) Polymerization and structure of nucleotide-free actin filaments. J Mol Biol 295:517-526.
37. Dickinson RB, Caro L, Purich DL (2004) Force generation by cytoskeletal filament end-tracking proteins. Biophys J 87:2838-2854.
38. Alberts JB, Odell GM (2004) In silico reconstitution of Listeria propulsion exhibits nano-saltation. PLoS Biol 2:e412.
39. Taylor KA, Tang J, Cheng Y, Winkler H (1997) The use of electron tomography for structural analysis of disordered protein arrays. J Struct Biol 120:372-386.
40. Bullock TL, Parthasarathy G, Kent H, Roberts TM, Stewart M (1996) New crystal forms of the motile major sperm protein (MSP) of Ascaris suum. J Struct Biol 116:432-437.