Assembly and turnover of short actin filaments by the formin INF2 and profilin

Journal of Biological Chemistry

Volumn 290, Issue 37, 2015, Pages 22494-22506

  Gurel, Pinar S ^a   Mu, A ^a   Guo, Bingqian ^b   Shu, Rui ^a   Mierke, Dale F ^b   Higgs, Henry N ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b Lamont Doherty Earth Observatory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEPOLYMERIZATION; MONOMERS; NUCLEOTIDES;

ACTIN FILAMENT; ACTIN NUCLEATION; BIOCHEMICAL EFFECTS; DIFFERENT MECHANISMS; MULTIPLE INTERACTIONS; NUCLEOTIDE EXCHANGE; PSEUDO-STEADY-STATE CONDITIONS; RATE-LIMITING STEPS;

PROTEINS;

ACTIN; ACTIN CAPPING PROTEIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CELL PROTEIN; CYTOCHALASIN D; INVERTED FORMIN 2 PROTEIN; LATRUNCULIN A; LATRUNCULIN B; PROFILIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; INF2 PROTEIN, HUMAN;

ARTICLE; COLORIMETRY; DEPOLYMERIZATION; ELECTRON MICROSCOPY; GENE AND NUCLEIC ACID PARAMETERS; HUMAN; HYDROLYSIS; NUCLEOTIDE EXCHANGE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTON NUCLEAR MAGNETIC RESONANCE; PSEUDO STEADY STATE; STEADY STATE; ACTIN FILAMENT; CHEMISTRY; GENETICS; PROTEIN FOLDING; PROTEIN MOTIF;

ACTIN CYTOSKELETON; AMINO ACID MOTIFS; HUMANS; MICROFILAMENT PROTEINS; PROFILINS; PROTEIN FOLDING;

EID: 84941585677     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.670166     Document Type: Article

References (47)

1. Chhabra, E. S., and Higgs, H. N. (2007) The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 9, 1110-1121
2. Blanchoin, L., and Pollard, T. D. (1999) Mechanism of interaction of Acanthamoeba actophorin (ADF/cofilin) with actin filaments. J. Biol. Chem. 274, 15538-15546
3. Theriot, J. A., and Mitchison, T. J. (1991) Actin microfilament dynamics in locomoting cells. Nature 352, 126-131
4. Ramabhadran, V., Korobova, F., Rahme, G. J., and Higgs, H. N. (2011) Splice variant-specific cellular function of the formin INF2 in maintenance of Golgi architecture. Mol. Biol. Cell 22, 4822-4833
5. Gurel, P. S., Hatch, A. L., and Higgs, H. N. (2014) Connecting the cytoskeleton to the endoplasmic reticulum and Golgi. Curr. Biol. 24, R660-R672
6. Miserey-Lenkei, S., Chalancon, G., Bardin, S., Formstecher, E., Goud, B., and Echard, A. (2010) Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat. Cell Biol. 12, 645-654
7. Pollard, T. D., and Cooper, J. A. (1986) Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu. Rev. Biochem. 55, 987-1035
8. Kovar, D. R., Harris, E. S., Mahaffy, R., Higgs, H. N., and Pollard, T. D. (2006) Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124, 423-435
9. Blanchoin, L., and Pollard, T. D. (2002) Hydrolysis of ATP by polymerized actin depends on the bound divalent cation but not profilin. Biochemistry 41, 597-602
10. Carlier, M. F., Pantaloni, D., Evans, J. A., Lambooy, P. K., Korn, E. D., and Webb, M. R. (1988) The hydrolysis of ATP that accompanies actin polymerization is essentially irreversible. FEBS Lett. 235, 211-214
11. Melki, R., Fievez, S., and Carlier, M. F. (1996) Continuous monitoring of Pi release following nucleotide hydrolysis in actin or tubulin assembly using 2-amino-6-mercapto-7-methylpurine ribonucleoside and purine-nucleoside phosphorylase as an enzyme-linked assay. Biochemistry 35, 12038-12045
12. Pollard, T. D., and Borisy, G. G. (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465
13. Pollard, T. D., and Cooper, J. A. (1984) Quantitative analysis of the effect of Acanthamoeba profilin on actin filament nucleation and elongation. Biochemistry 23, 6631-6641
14. Pantaloni, D., and Carlier, M. F. (1993) How profilin promotes actin filament assembly in the presence of thymosin beta 4. Cell 75, 1007-1014
15. Pring, M., Weber, A., and Bubb, M. R. (1992) Profilin-actin complexes directly elongate actin filaments at the barbed end. Biochemistry 31, 1827-1836
16. Campellone, K. G., and Welch, M. D. (2010) A nucleator arms race: cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 11, 237-251
17. Chesarone, M. A., and Goode, B. L. (2009) Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 21, 28-37
18. Mockrin, S. C., and Korn, E. D. (1980) Acanthamoeba profilin interacts with G-actin to increase the rate of exchange of actin-bound adenosine 5-triphosphate. Biochemistry 19, 5359-5362
19. Vinson, V. K., De La Cruz, E. M., Higgs, H. N., and Pollard, T. D. (1998) Interactions of Acanthamoeba profilin with actin and nucleotides bound to actin. Biochemistry 37, 10871-10880
20. Selden, L. A., Kinosian, H. J., Estes, J. E., and Gershman, L. C. (1999) Impact of profilin on actin-bound nucleotide exchange and actin polymerization dynamics. Biochemistry 38, 2769-2778
21. Paul, A. S., and Pollard, T. D. (2009) Review of the mechanism of processive actin filament elongation by formins. Cell Motil. Cytoskeleton 66, 606-617
22. Li, F., and Higgs, H. N. (2003) The mouse formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr. Biol. 13, 1335-1340
23. Chhabra, E. S., and Higgs, H. N. (2006) INF2 Is a WASP homology 2 motif-containing formin that severs actin filaments and accelerates both polymerization and depolymerization. J. Biol. Chem. 281, 26754-26767
24. Heimsath, E. G., Jr., and Higgs, H. N. (2012) The C terminus of formin FMNL3 accelerates actin polymerization and contains a WH2 domainlike sequence that binds both monomers and filament barbed ends. J. Biol. Chem. 287, 3087-3098
25. Gurel, P. S., Ge, P., Grintsevich, E. E., Shu, R., Blanchoin, L., Zhou, Z. H., Reisler, E., and Higgs, H. N. (2014) INF2-mediated severing through actin filament encirclement and disruption. Curr. Biol. 24, 156-164
26. Korobova, F., Ramabhadran, V., and Higgs, H. N. (2013) An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 339, 464-467
27. Hakes, D. J., and Dixon, J. E. (1992) New vectors for high level expression of recombinant proteins in bacteria. Anal. Biochem. 202, 293-298
28. Ramabhadran, V., Gurel, P. S., and Higgs, H. N. (2012) Mutations to the formin homology 2 domain of INF2 protein have unexpected effects on actin polymerization and severing. J. Biol. Chem. 287, 34234-34245
29. Li, F., and Higgs, H. N. (2005) Dissecting requirements for auto-inhibition of actin nucleation by the formin, mDia1. J. Biol. Chem. 280, 6986-6992
30. Harris, E. S., Li, F., and Higgs, H. N. (2004) The mouse formin, FRLa, slows actin filament barbed end elongation, competes with capping protein, accelerates polymerization from monomers, and severs filaments J. Biol. Chem. 279, 20076-20087
31. Spudich, J. A., and Watt, S. (1971) The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosintroponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246, 4866-4871
32. Cooper, J. A., Walker, S. B., and Pollard, T. D. (1983) Pyrene actin: documentation of the validity of a sensitive assay for actin polymerization. J. Muscle Res. Cell Motil. 4, 253-262
33. Isambert, H., Venier, P., Maggs, A. C., Fattoum, A., Kassab, R., Pantaloni, D., and Carlier, M. F. (1995) Flexibility of actin filaments derived from thermal fluctuations. Effect of bound nucleotide, phalloidin, and muscle regulatory proteins. J. Biol. Chem. 270, 11437-11444
34. Guo, B., Gurel, P. S., Shu, R., Higgs, H. N., Pellegrini, M., and Mierke, D. F. (2014) Monitoring ATP hydrolysis and ATPase inhibitor screening using 1H NMR. Chem. Commun. (Camb.) 50, 12037-12039
35. Leonard, M., Song, B. D., Ramachandran, R., and Schmid, S. L. (2005) Robust colorimetric assays for dynamin's basal and stimulated GTPase activities. Methods Enzymol. 404, 490-503
36. Bubb, M. R., Lewis, M. S., and Korn, E. D. (1991) The interaction of monomeric actin with two binding sites on Acanthamoeba actobindin. J. Biol. Chem. 266, 3820-3826
37. Gell, C., Bormuth, V., Brouhard, G. J., Cohen, D. N., Diez, S., Friel, C. T., Helenius, J., Nitzsche, B., Petzold, H., Ribbe, J., Schäffer, E., Stear, J. H., Trushko, A., Varga, V., Widlund, P. O., Zanic, M., and Howard, J. (2010) Microtubule dynamics reconstituted in vitro and imaged by single-molecule fluorescence microscopy. Methods Cell Biol. 95, 221-245
38. Pollard, T. D., Blanchoin, L., and Mullins, R. D. (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29, 545-576
39. McCullagh, M., Saunders, M. G., and Voth, G. A. (2014) Unraveling the mystery of ATP hydrolysis in actin filaments. J. Am. Chem. Soc. 136, 13053-13058
40. Pollard, T. D. (1986) Rate constants for the reactions of ATP- and ADPactin with the ends of actin filaments. J. Cell Biol. 103, 2747-2754
41. Lu, J., and Pollard, T. D. (2001) Profilin binding to poly-L-proline and actin monomers along with ability to catalyze actin nucleotide exchange is required for viability of fission yeast. Mol. Biol. Cell 12, 1161-1175
42. Goddette, D. W., and Frieden, C. (1986) Actin polymerization. The mechanism of action of cytochalasin D. J. Biol. Chem. 261, 15974-15980
43. Husson, C., Renault, L., Didry, D., Pantaloni, D., and Carlier, M. F. (2011) Cordon-Bleu uses WH2 domains as multifunctional dynamizers of actin filament assembly. Mol. Cell 43, 464-477
44. Ohm, T., and Wegner, A. (1994) Mechanism of ATP hydrolysis by polymeric actin. Biochim. Biophys. Acta 1208, 8-14
45. Jégou, A., Niedermayer, T., Orbán, J., Didry, D., Lipowsky, R., Carlier, M. F., and Romet-Lemonne, G. (2011) Individual actin filaments in a microfluidic flow reveal the mechanism of ATP hydrolysis and give insight into the properties of profilin. PLoS Biol. 9, e1001161
46. Hatch, A. L., Gurel, P. S., and Higgs, H. N. (2014) Novel roles for actin in mitochondrial fission. J. Cell Sci. 127, 4549-4560
47. Chhabra, E. S., Ramabhadran, V., Gerber, S. A., and Higgs, H. N. (2009) INF2 is an endoplasmic reticulum-associated formin protein. J. Cell Sci. 122, 1430-1440