Regulatory Mimicry in Listeria monocytogenes Actin-Based Motility

Cell Host and Microbe

Volumn 6, Issue 3, 2009, Pages 268-278

  Chong, Ryan ^a   Swiss, Rachel ^a   Briones, Gabriel ^a   Stone, Kathryn L ^b   Gulcicek, Erol E ^b   Agaisse, Hervé ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CELLBIO; MICROBIO

Indexed keywords

ACTA PROTEIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; CK2 PROTEIN; PROTEIN SERINE THREONINE KINASE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; WAVE PROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN;

ACTIN POLYMERIZATION; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOSKELETON; FEMALE; IMAGE ANALYSIS; INTRACELLULAR BACTERIUM; LISTERIA MONOCYTOGENES; MICROBIAL KINETICS; MOLECULAR MIMICRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RNA INTERFERENCE; STRUCTURAL HOMOLOGY;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CASEIN KINASE II; FEMALE; HELA CELLS; HUMANS; LISTERIA INFECTIONS; LISTERIA MONOCYTOGENES; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

EID: 69949176832     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2009.08.006     Document Type: Article

References (42)

1. Arnaud M., Chastanet A., and Debarbouille M. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl. Environ. Microbiol. 70 (2004) 6887-6891
2. Bi E., and Zigmond S.H. Actin polymerization: Where the WASP stings. Curr. Biol. 9 (1999) R160-R163
3. Boujemaa-Paterski R., Gouin E., Hansen G., Samarin S., Le Clainche C., Didry D., Dehoux P., Cossart P., Kocks C., Carlier M.F., et al. Listeria protein ActA mimics WASp family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry 40 (2001) 11390-11404
4. Brundage R.A., Smith G.A., Camilli A., Theriot J.A., and Portnoy D.A. Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc. Natl. Acad. Sci. USA 90 (1993) 11890-11894
5. Campellone K.G., Webb N.J., Znameroski E.A., and Welch M.D. WHAMM is an Arp2/3 complex activator that binds microtubules and functions in ER to Golgi transport. Cell 134 (2008) 148-161
6. Cory G.O., Cramer R., Blanchoin L., and Ridley A.J. Phosphorylation of the WASP-VCA domain increases its affinity for the Arp2/3 complex and enhances actin polymerization by WASP. Mol. Cell 11 (2003) 1229-1239
7. Derry J.M., Ochs H.D., and Francke U. Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell 78 (1994) 635-644
8. Domann E., Wehland J., Rohde M., Pistor S., Hartl M., Goebel W., Leimeister-Wachter M., Wuenscher M., and Chakraborty T. A novel bacterial virulence gene in Listeria monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin. EMBO J. 11 (1992) 1981-1990
9. Fillat C., Espanol T., Oset M., Ferrando M., Estivill X., and Volpini V. Identification of WASP mutations in 14 Spanish families with Wiskott-Aldrich syndrome. Am. J. Med. Genet. 100 (2001) 116-121
10. Goley E.D., and Welch M.D. The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7 (2006) 713-726
11. Goley E.D., Ohkawa T., Mancuso J., Woodruff J.B., D'Alessio J.A., Cande W.Z., Volkman L.E., and Welch M.D. Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WASP-like protein. Science 314 (2006) 464-467
12. Gouin E., Egile C., Dehoux P., Villiers V., Adams J., Gertler F., Li R., and Cossart P. The RickA protein of Rickettsia conorii activates the Arp2/3 complex. Nature 427 (2004) 457-461
13. Gouin E., Welch M.D., and Cossart P. Actin-based motility of intracellular pathogens. Curr. Opin. Microbiol. 8 (2005) 35-45
14. Jeng R.L., Goley E.D., D'Alessio J.A., Chaga O.Y., Svitkina T.M., Borisy G.G., Heinzen R.A., and Welch M.D. A Rickettsia WASP-like protein activates the Arp2/3 complex and mediates actin-based motility. Cell. Microbiol. 6 (2004) 761-769
15. Kocks C., Gouin E., Tabouret M., Berche P., Ohayon H., and Cossart P. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68 (1992) 521-531
16. Kolluri R., Shehabeldin A., Peacocke M., Lamhonwah A.M., Teichert-Kuliszewska K., Weissman S.M., and Siminovitch K.A. Identification of WASP mutations in patients with Wiskott-Aldrich syndrome and isolated thrombocytopenia reveals allelic heterogeneity at the WAS locus. Hum. Mol. Genet. 4 (1995) 1119-1126
17. Lambrechts A., Gevaert K., Cossart P., Vandekerckhove J., and Van Troys M. Listeria comet tails: the actin-based motility machinery at work. Trends Cell Biol. 18 (2008) 220-227
18. Lasa I., David V., Gouin E., Marchand J.B., and Cossart P. The amino-terminal part of ActA is critical for the actin-based motility of Listeria monocytogenes; the central proline-rich region acts as a stimulator. Mol. Microbiol. 18 (1995) 425-436
19. Lasa I., Gouin E., Goethals M., Vancompernolle K., David V., Vandekerckhove J., and Cossart P. Identification of two regions in the N-terminal domain of ActA involved in the actin comet tail formation by Listeria monocytogenes. EMBO J. 16 (1997) 1531-1540
20. Lauer P., Theriot J.A., Skoble J., Welch M.D., and Portnoy D.A. Systematic mutational analysis of the amino-terminal domain of the Listeria monocytogenes ActA protein reveals novel functions in actin-based motility. Mol. Microbiol. 42 (2001) 1163-1177
21. Linardopoulou E.V., Parghi S.S., Friedman C., Osborn G.E., Parkhurst S.M., and Trask B.J. Human subtelomeric WASH genes encode a new subclass of the WASP family. PLoS Genet. 3 (2007) e237
22. Machesky L.M., and Insall R.H. Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8 (1998) 1347-1356
23. Machesky L.M., Insall R.H., and Volkman L.E. WASP homology sequences in baculoviruses. Trends Cell Biol. 11 (2001) 286-287
24. Marchand J.B., Kaiser D.A., Pollard T.D., and Higgs H.N. Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat. Cell Biol. 3 (2001) 76-82
25. Niebuhr K., Ebel F., Frank R., Reinhard M., Domann E., Carl U.D., Walter U., Gertler F.B., Wehland J., and Chakraborty T. A novel proline-rich motif present in ActA of Listeria monocytogenes and cytoskeletal proteins is the ligand for the EVH1 domain, a protein module present in the Ena/VASP family. EMBO J. 16 (1997) 5433-5444
26. Panchal S.C., Kaiser D.A., Torres E., Pollard T.D., and Rosen M.K. A conserved amphipathic helix in WASP/Scar proteins is essential for activation of Arp2/3 complex. Nat. Struct. Biol. 10 (2003) 591-598
27. Pinna L.A. Protein kinase CK2: a challenge to canons. J. Cell Sci. 115 (2002) 3873-3878
28. Pistor S., Grobe L., Sechi A.S., Domann E., Gerstel B., Machesky L.M., Chakraborty T., and Wehland J. Mutations of arginine residues within the 146-KKRRK-150 motif of the ActA protein of Listeria monocytogenes abolish intracellular motility by interfering with the recruitment of the Arp2/3 complex. J. Cell Sci. 113 (2000) 3277-3287
29. Pocha S.M., and Cory G.O. WAVE2 is regulated by multiple phosphorylation events within its VCA domain. Cell Motil. Cytoskeleton 66 (2009) 36-47
30. Pollard T.D. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36 (2007) 451-477
31. Rohatgi R., Ma L., Miki H., Lopez M., Kirchhausen T., Takenawa T., and Kirschner M.W. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97 (1999) 221-231
32. Schlech III W.F. Listeria gastroenteritis-old syndrome, new pathogen. N. Engl. J. Med. 336 (1997) 130-132
33. Skoble J., Portnoy D.A., and Welch M.D. Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J. Cell Biol. 150 (2000) 527-538
34. Smith G.A., Theriot J.A., and Portnoy D.A. The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. J. Cell Biol. 135 (1996) 647-660
35. Stebbins C.E., and Galan J.E. Structural mimicry in bacterial virulence. Nature 412 (2001) 701-705
36. Stevens J.M., Galyov E.E., and Stevens M.P. Actin-dependent movement of bacterial pathogens. Nat. Rev. Microbiol. 4 (2006) 91-101
37. Takenawa T., and Suetsugu S. The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 8 (2007) 37-48
38. Tilney L.G., and Portnoy D.A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109 (1989) 1597-1608
39. Welch M.D., Iwamatsu A., and Mitchison T.J. Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385 (1997) 265-269
40. Welch M.D., Rosenblatt J., Skoble J., Portnoy D.A., and Mitchison T.J. Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281 (1998) 105-108
41. Zalevsky J., Grigorova I., and Mullins R.D. Activation of the Arp2/3 complex by the Listeria acta protein. Acta binds two actin monomers and three subunits of the Arp2/3 complex. J. Biol. Chem. 276 (2001) 3468-3475
42. Zuchero J.B., Coutts A.S., Quinlan M.E., Thangue N.B., and Mullins R.D. p53-cofactor JMY is a multifunctional actin nucleation factor. Nat. Cell Biol. 11 (2009) 451-459