Bacterial subversion of host cytoskeletal machinery: Hijacking formins and the Arp2/3 complex

BioEssays

Volumn 36, Issue 7, 2014, Pages 687-696

  Truong, Dorothy ^a,b   Copeland, John W ^c   Brumell, John H ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Actin based motility; Arp2 3; Formins; Host pathogen interactions

Indexed keywords

ACTIN BINDING PROTEIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; BACTERIAL PROTEIN; CYTOCHALASIN D; F ACTIN; FMNL1 PROTEIN; FORMIN PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; BORRELIA BURGDORFERI; CONFORMATIONAL TRANSITION; CYTOSKELETON; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; IN VITRO STUDY; LYME DISEASE; MACROPHAGE; NONHUMAN; PHAGOCYTOSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; RICKETTSIA; SALMONELLA TYPHIMURIUM; SCANNING ELECTRON MICROSCOPY; SHIGELLA; SHIGELLA FLEXNERI; STRESS FIBER; TICK BITE; TRANSPOSON; XENOPUS; XENOPUS LAEVIS; ANIMAL; BACTERIA; METABOLISM; PATHOGENICITY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS);

ACTIN CYTOSKELETON; ACTIN-RELATED PROTEIN 2-3 COMPLEX; ANIMALS; BACTERIA; CYTOSKELETON; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROFILAMENT PROTEINS;

EID: 84901927417     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400038     Document Type: Review

References (120)

1. Rotty JD, Wu C, Bear JE. 2013. New insights into the regulation and cellular functions of the ARP2/3 complex. Nat Rev Mol Cell Biol 14: 7-12.
2. Bugyi B, Carlier MF. 2010. Control of actin filament treadmilling in cell motility. Annu Rev Biophys 39: 449-70.
3. Firat-Karalar EN, Welch MD. 2011. New mechanisms and functions of actin nucleation. Curr Opin Cell Biol 23: 4-13.
4. Machesky LM, Atkinson SJ, Ampe C, Vandekerckhove J, et al. 1994. Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J Cell Biol 127: 107-15.
5. Kelleher JF, Atkinson SJ, Pollard TD. 1995. Sequences, structural models, and cellular localization of the actin-related proteins Arp2 and Arp3 from Acanthamoeba. J Cell Biol 131: 385-97.
6. Amann KJ, Pollard TD. 2001. Direct real-time observation of actin filament branching mediated by Arp2/3 complex using total internal reflection fluorescence microscopy. Proc Natl Acad Sci USA 98: 15009-13.
7. Mullins RD, Heuser JA, Pollard TD. 1998. The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci USA 95: 6181-6.
8. Goley ED, Rodenbusch SE, Martin AC, Welch MD. 2004. Critical conformational changes in the Arp2/3 complex are induced by nucleotide and nucleation promoting factor. Mol Cell 16: 269-79.
9. Stradal TE, Scita G. 2006. Protein complexes regulating Arp2/3-mediated actin assembly. Curr Opin Cell Biol 18: 4-10.
10. Padrick SB, Doolittle LK, Brautigam CA, King DS, et al. 2011. Arp2/3 complex is bound and activated by two WASP proteins. Proc Natl Acad Sci USA 108: E472-9.
11. Ti SC, Jurgenson CT, Nolen BJ, Pollard TD. 2011. Structural and biochemical characterization of two binding sites for nucleation-promoting factor WASp-VCA on Arp2/3 complex. Proc Natl Acad Sci USA 108: E463-71.
12. Rodal AA, Sokolova O, Robins DB, Daugherty KM, et al. 2005. Conformational changes in the Arp2/3 complex leading to actin nucleation. Nat Struct Mol Biol 12: 26-31.
13. Helgeson LA, Nolen BJ. 2013. Mechanism of synergistic activation of Arp2/3 complex by cortactin and N-WASP. Elife 2: e00884.
14. Woychik RP, Maas RL, Zeller R, Vogt TF, et al. 1990. 'Formins': proteins deduced from the alternative transcripts of the limb deformity gene. Nature 346: 850-3.
15. Castrillon DH, Wasserman SA. 1994. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120: 3367-77.
16. Higgs HN. 2005. Formin proteins: a domain-based approach. Trends Biochem Sci 30: 342-53.
17. Schonichen A, Geyer M. 2010. Fifteen formins for an actin filament: a molecular view on the regulation of human formins. Biochim Biophys Acta 1803: 152-63.
18. Copeland JW, Copeland SJ, Treisman R. 2004. Homo-oligomerization is essential for F-actin assembly by the formin family FH2 domain. J Biol Chem 279: 50250-6.
19. Shimada A, Nyitrai M, Vetter IR, Kuhlmann D, et al. 2004. The core FH2 domain of diaphanous-related formins is an elongated actin binding protein that inhibits polymerization. Mol Cell 13: 511-22.
20. Xu Y, Moseley JB, Sagot I, Poy F, et al. 2004. Crystal structures of a formin homology-2 domain reveal a tethered dimer architecture. Cell 116: 711-23.
21. Lu J, Meng W, Poy F, Maiti S, et al. 2007. Structure of the FH2 domain of Daam1: implications for formin regulation of actin assembly. J Mol Biol 369: 1258-69.
22. Harris ES, Gauvin TJ, Heimsath EG, Higgs HN. 2010. Assembly of filopodia by the formin FRL2 (FMNL3). Cytoskeleton 67: 755-72.
23. Harris ES, Rouiller I, Hanein D, Higgs HN. 2006. Mechanistic differences in actin bundling activity of two mammalian formins, FRL1 and mDia2. J Biol Chem 281: 14383-92.
24. Bartolini F, Moseley JB, Schmoranzer J, Cassimeris L, et al. 2008. The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J Cell Biol 181: 523-36.
25. Scott BJ, Neidt EM, Kovar DR. 2011. The functionally distinct fission yeast formins have specific actin-assembly properties. Mol Biol Cell 22: 3826-39.
26. Ishizaki T, Morishima Y, Okamoto M, Furuyashiki T, et al. 2001. Coordination of microtubules and the actin cytoskeleton by the Rho effector mDia1. Nat Cell Biol 3: 8-14.
27. Thompson ME, Heimsath EG, Gauvin TJ, Higgs HN, et al. 2013. FMNL3 FH2-actin structure gives insight into formin-mediated actin nucleation and elongation. Nat Struct Mol Biol 20: 111-8.
28. Pring M, Evangelista M, Boone C, Yang C, et al. 2003. Mechanism of formin-induced nucleation of actin filaments. Biochemistry 42: 486-96.
29. Romero S, Le Clainche C, Didry D, Egile C, et al. 2004. Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119: 419-29.
30. Higashida C, Miyoshi T, Fujita A, Oceguera-Yanez F, et al. 2004. Actin polymerization-driven molecular movement of mDia1 in living cells. Science 303: 2007-10.
31. Kovar DR, Pollard TD. 2004. Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc Natl Acad Sci USA 101: 14725-30.
32. Mizuno H, Higashida C, Yuan Y, Ishizaki T, et al. 2011. Rotational movement of the formin mDia1 along the double helical strand of an actin filament. Science 331: 80-3.
33. Zigmond SH, Evangelista M, Boone C, Yang C, et al. 2003. Formin leaky cap allows elongation in the presence of tight capping proteins. Curr Biol 13: 1820-3.
34. Shemesh T, Otomo T, Rosen MK, Bershadsky AD, et al. 2005. A novel mechanism of actin filament processive capping by formin: solution of the rotation paradox. J Cell Biol 170: 889-93.
35. Paul AS, Pollard TD. 2009. Review of the mechanism of processive actin filament elongation by formins. Cell Motil Cytoskeleton 66: 606-17.
36. Harris ES, Li F, Higgs HN. 2004. The mouse formin, FRLalpha, slows actin filament barbed end elongation, competes with capping protein, accelerates polymerization from monomers, and severs filaments. J Biol Chem 279: 20076-87.
37. Heimsath EG, Jr., Higgs HN. 2012. The C terminus of formin FMNL3 accelerates actin polymerization and contains a WH2 domain-like sequence that binds both monomers and filament barbed ends. J Biol Chem 287: 3087-98.
38. Gould CJ, Maiti S, Michelot A, Graziano BR, et al. 2011. The formin DAD domain plays dual roles in autoinhibition and actin nucleation. Curr Biol 21: 384-90.
39. Vaillant DC, Copeland SJ, Davis C, Thurston SF, et al. 2008. Interaction of the N- and C-terminal autoregulatory domains of FRL2 does not inhibit FRL2 activity. J Biol Chem 283: 33750-62.
40. Gurel PS, Ge P, Grintsevich EE, Shu R, et al. 2014. INF2-mediated severing through actin filament encirclement and disruption. Curr Biol 24: 156-64.
41. Ramabhadran V, Gurel PS, Higgs HN. 2012. Mutations to the formin homology 2 domain of INF2 protein have unexpected effects on actin polymerization and severing. J Biol Chem 287: 34234-45.
42. Bartolini F, Ramalingam N, Gundersen GG. 2012. Actin-capping protein promotes microtubule stability by antagonizing the actin activity of mDia1. Mol Biol Cell 23: 4032-40.
43. Roth-Johnson EA, Vizcarra CL, Bois JS, Quinlan ME. 2014. Interaction between microtubules and the Drosophila formin Cappuccino and its effect on actin assembly. J Biol Chem 289: 4395-404.
44. Gaillard J, Ramabhadran V, Neumanne E, Gurel P, et al. 2011. Differential interactions of the formins INF2, mDia1, and mDia2 with microtubules. Mol Biol Cell 22: 4575-87.
45. Young KG, Thurston SF, Copeland S, Smallwood C, et al. 2008. INF1 is a novel microtubule-associated formin. Mol Biol Cell 19: 5168-80.
46. Thurston SF, Kulacz WA, Shaikh S, Lee JM, et al. 2012. The ability to induce microtubule acetylation is a general feature of formin proteins. PLoS One 7: e48041.
47. Copeland SJ, Green BJ, Burchat S, Papalia GA, et al. 2007. The diaphanous inhibitory domain/diaphanous autoregulatory domain interaction is able to mediate heterodimerization between mDia1 and mDia2. J Biol Chem 282: 30120-30.
48. Maiti S, Michelot A, Gould C, Blanchoin L, et al. 2012. Structure and activity of full-length formin mDia1. Cytoskeleton 69: 393-405.
49. Nezami A, Poy F, Toms A, Zheng W, et al. 2010. Crystal structure of a complex between amino and carboxy terminal fragments of mDia1: insights into autoinhibition of diaphanous-related formins. PLoS One 5: e12992.
50. Alberts AS. 2001. Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain. J Biol Chem 276: 2824-30.
51. Li F, Higgs HN. 2003. The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr Biol 13: 1335-40.
52. Kobielak A, Pasolli HA, Fuchs E. 2004. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat Cell Biol 6: 21-30.
53. Ramabhadran V, Hatch AL, Higgs HN. 2013. Actin monomers activate inverted formin 2 by competing with its autoinhibitory interaction. J Biol Chem 288: 26847-55.
54. Quinlan ME, Hilgert S, Bedrossian A, Mullins RD, et al. 2007. Regulatory interactions between two actin nucleators, Spire and Cappuccino. J Cell Biol 179: 117-28.
55. Otomo T, Otomo C, Tomchick DR, Machius M, et al. 2005. Structural basis of Rho GTPase-mediated activation of the formin mDia1. Mol Cell 18: 273-81.
56. Li F, Higgs HN. 2005. Dissecting requirements for auto-inhibition of actin nucleation by the formin, mDia1. J Biol Chem 280: 6986-92.
57. Nezami AG, Poy F, Eck MJ. 2006. Structure of the autoinhibitory switch in formin mDia1. Structure 14: 257-63.
58. Rose R, Weyand M, Lammers M, Ishizaki T, et al. 2005. Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature 435: 513-8.
59. Gasteier JE, Madrid R, Krautkramer E, Schroder S, et al. 2003. Activation of the Rac-binding partner FHOD1 induces actin stress fibers via a ROCK-dependent mechanism. J Biol Chem 278: 38902-12.
60. Takeya R, Taniguchi K, Narumiya S, Sumimoto H. 2008. The mammalian formin FHOD1 is activated through phosphorylation by ROCK and mediates thrombin-induced stress fibre formation in endothelial cells. EMBO J 27: 618-28.
61. Staus DP, Taylor JM, Mack CP. 2011. Enhancement of mDia2 activity by Rho-kinase-dependent phosphorylation of the diaphanous autoregulatory domain. Biochem J 439: 57-65.
62. Truong D, Brabant D, Bashkurov M, Wan LC, et al. 2013. Formin-mediated actin polymerization promotes Salmonella invasion. Cell Microbiol 15: 2051-63.
63. Wang Y, El-Zaru MR, Surks HK, Mendelsohn ME. 2004. Formin homology domain protein (FHOD1) is a cyclic GMP-dependent protein kinase I-binding protein and substrate in vascular smooth muscle cells. J Biol Chem 279: 24420-6.
64. Iskratsch T, Lange S, Dwyer J, Kho AL, et al. 2010. Formin follows function: a muscle-specific isoform of FHOD3 is regulated by CK2 phosphorylation and promotes myofibril maintenance. J Cell Biol 191: 1159-72.
65. Cheng L, Zhang J, Ahmad S, Rozier L, et al. 2011. Aurora B regulates formin mDia3 in achieving metaphase chromosome alignment. Dev Cell 20: 342-52.
66. Gorelik R, Yang C, Kameswaran V, Dominguez R, et al. 2011. Mechanisms of plasma membrane targeting of formin mDia2 through its amino terminal domains. Mol Biol Cell 22: 189-201.
67. Seth A, Otomo C, Rosen MK. 2006. Autoinhibition regulates cellular localization and actin assembly activity of the diaphanous-related formins FRLalpha and mDia1. J Cell Biol 174: 701-13.
68. Block J, Breitsprecher D, Kuhn S, Winterhoff M, et al. 2012. FMNL2 drives actin-based protrusion and migration downstream of Cdc42. Curr Biol 22: 1005-12.
69. Han Y, Eppinger E, Schuster IG, Weigand LU, et al. 2009. Formin-like 1 (FMNL1) is regulated by N-terminal myristoylation and induces polarized membrane blebbing. J Biol Chem 284: 33409-17.
70. Moriya K, Yamamoto T, Takamitsu E, Matsunaga Y, et al. 2012. Protein N-myristoylation is required for cellular morphological changes induced by two formin family proteins, FMNL2 and FMNL3. Biosci Biotechnol Biochem 76: 1201-9.
71. Jegou A, Carlier MF, Romet-Lemonne G. 2013. Formin mDia1 senses and generates mechanical forces on actin filaments. Nat Commun 4: 1883.
72. Courtemanche N, Lee JY, Pollard TD, Greene EC. 2013. Tension modulates actin filament polymerization mediated by formin and profilin. Proc Natl Acad Sci USA 110: 9752-7.
73. Chan MW, Chaudary F, Lee W, Copeland JW, et al. 2010. Force-induced myofibroblast differentiation through collagen receptors is dependent on mammalian diaphanous (mDia). J Biol Chem 285: 9273-81.
74. Higashida C, Kiuchi T, Akiba Y, Mizuno H, et al. 2013. F- and G-actin homeostasis regulates mechanosensitive actin nucleation by formins. Nat Cell Biol 15: 395-405.
75. Watanabe N, Kato T, Fujita A, Ishizaki T, et al. 1999. Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1: 136-43.
76. Hotulainen P, Lappalainen P. 2006. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 173: 383-94.
77. Oakes PW, Beckham Y, Stricker J, Gardel ML. 2012. Tension is required but not sufficient for focal adhesion maturation without a stress fiber template. J Cell Biol 196: 363-74.
78. Schulze N, Graessl M, Blancke Soares A, Geyer M, et al. 2014. FHOD1 regulates stress fiber organization by controlling transversal arc and dorsal fiber dynamics. J Cell Sci 127: 1379-93.
79. Bosch M, Le KH, Bugyi B, Correia JJ, et al. 2007. Analysis of the function of Spire in actin assembly and its synergy with formin and profilin. Mol Cell 28: 555-68.
80. Pfender S, Kuznetsov V, Pleiser S, Kerkhoff E, et al. 2011. Spire-type actin nucleators cooperate with Formin-2 to drive asymmetric oocyte division. Curr Biol 21: 955-60.
81. Okada K, Bartolini F, Deaconescu AM, Moseley JB, et al. 2010. Adenomatous polyposis coli protein nucleates actin assembly and synergizes with the formin mDia1. J Cell Biol 189: 1087-96.
82. Beli P, Mascheroni D, Xu D, Innocenti M. 2008. WAVE and Arp2/3 jointly inhibit filopodium formation by entering into a complex with mDia2. Nat Cell Biol 10: 849-57.
83. Sarmiento C, Wang W, Dovas A, Yamaguchi H, et al. 2008. WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J Cell Biol 180: 1245-60.
84. Suraneni P, Rubinstein B, Unruh JR, Durnin M, et al. 2012. The Arp2/3 complex is required for lamellipodia extension and directional fibroblast cell migration. J Cell Biol 197: 239-51.
85. Tojkander S, Gateva G, Schevzov G, Hotulainen P, et al. 2011. A molecular pathway for myosin II recruitment to stress fibers. Curr Biol 21: 539-50.
86. Lee K, Gallop JL, Rambani K, Kirschner MW. 2010. Self-assembly of filopodia-like structures on supported lipid bilayers. Science 329: 1341-5.
87. Yang C, Czech L, Gerboth S, Kojima S, et al. 2007. Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol 5: e317.
88. Stevens JM, Galyov EE, Stevens MP. 2006. Actin-dependent movement of bacterial pathogens. Nat Rev Microbiol 4: 91-101.
89. Welch MD, Iwamatsu A, Mitchison TJ. 1997. Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385: 265-9.
90. Welch MD, Rosenblatt J, Skoble J, Portnoy DA, et al. 1998. Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281: 105-8.
91. Kocks C, Gouin E, Tabouret M, Berche P, et al. 1992. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68: 521-31.
92. Kubori T, Matsushima Y, Nakamura D, Uralil J, et al. 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602-5.
93. Finlay BB, Ruschkowski S, Dedhar S. 1991. Cytoskeletal rearrangements accompanying salmonella entry into epithelial cells. J Cell Sci 99(Pt 2): 283-96.
94. Patel JC, Galan JE. 2006. Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J Cell Biol 175: 453-63.
95. Zhou D, Chen LM, Hernandez L, Shears SB, et al. 2001. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol 39: 248-59.
96. Stender S, Friebel A, Linder S, Rohde M, et al. 2000. Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol Microbiol 36: 1206-21.
97. Hardt WD, Chen LM, Schuebel KE, Bustelo XR, et al. 1998. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815-26.
98. Rottner K, Hanisch J, Campellone KG. WASH, WHAMM and JMY: regulation of Arp2/3 complex and beyond. Trends Cell Biol 20: 650-61.
99. Radolf JD, Caimano MJ, Stevenson B, Hu LT. 2012. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat Rev Microbiol 10: 87-99.
100. Linder S, Heimerl C, Fingerle V, Aepfelbacher M, et al. 2001. Coiling phagocytosis of Borrelia burgdorferi by primary human macrophages is controlled by CDC42Hs and Rac1 and involves recruitment of Wiskott-Aldrich syndrome protein and Arp2/3 complex. Infect Immun 69: 1739-46.
101. Naj X, Hoffmann AK, Himmel M, Linder S. 2013. The formins FMNL1 and mDia1 regulate coiling phagocytosis of Borrelia burgdorferi by primary human macrophages. Infect Immun 81: 1683-95.
102. Horwitz MA. 1984. Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell 36: 27-33.
103. Neumann AK, Jacobson K. 2010. A novel pseudopodial component of the dendritic cell anti-fungal response: the fungipod. PLoS Pathog 6: e1000760.
104. Gouin E, Gantelet H, Egile C, Lasa I, et al. 1999. A comparative study of the actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J Cell Sci 112(Pt 11): 1697-708.
105. Schroeder GN, Hilbi H. 2008. Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion. Clin Microbiol Rev 21: 134-56.
106. Egile C, Loisel TP, Laurent V, Li R, et al. 1999. Activation of the CDC42 effector N-WASP by the Shigella flexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility. J Cell Biol 146: 1319-32.
107. Kadurugamuwa JL, Rohde M, Wehland J, Timmis KN. 1991. Intercellular spread of Shigella flexneri through a monolayer mediated by membranous protrusions and associated with reorganization of the cytoskeletal protein vinculin. Infect Immun 59: 3463-71.
108. Heindl JE, Saran I, Yi CR, Lesser CF, et al. 2010. Requirement for formin-induced actin polymerization during spread of Shigella flexneri. Infect Immun 78: 193-203.
109. Watanabe N, Madaule P, Reid T, Ishizaki T, et al. 1997. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 16: 3044-56.
110. Gouin E, Egile C, Dehoux P, Villiers V, et al. 2004. The RickA protein of Rickettsia conorii activates the Arp2/3 complex. Nature 427: 457-61.
111. Jeng RL, Goley ED, D'Alessio JA, Chaga OY, et al. 2004. A Rickettsia WASP-like protein activates the Arp2/3 complex and mediates actin-based motility. Cell Microbiol 6: 761-9.
112. Harlander RS, Way M, Ren Q, Howe D, et al. 2003. Effects of ectopically expressed neuronal Wiskott-Aldrich syndrome protein domains on Rickettsia rickettsii actin-based motility. Infect Immun 71: 1551-6.
113. Serio AW, Jeng RL, Haglund CM, Reed SC, et al. 2010. Defining a core set of actin cytoskeletal proteins critical for actin-based motility of Rickettsia. Cell Host Microbe 7: 388-98.
114. Van Kirk LS, Hayes SF, Heinzen RA. 2000. Ultrastructure of Rickettsia rickettsii actin tails and localization of cytoskeletal proteins. Infect Immun 68: 4706-13.
115. Blanc G, Ngwamidiba M, Ogata H, Fournier PE, et al. 2005. Molecular evolution of rickettsia surface antigens: evidence of positive selection. Mol Biol Evol 22: 2073-83.
116. Haglund CM, Choe JE, Skau CT, Kovar DR, et al. 2010. Rickettsia Sca2 is a bacterial formin-like mediator of actin-based motility. Nat Cell Biol 12: 1057-63.
117. Kleba B, Clark TR, Lutter EI, Ellison DW, et al. 2010. Disruption of the Rickettsia rickettsii Sca2 autotransporter inhibits actin-based motility. Infect Immun 78: 2240-7.
118. Madasu Y, Suarez C, Kast DJ, Kovar DR, et al. 2013. Rickettsia Sca2 has evolved formin-like activity through a different molecular mechanism. Proc Natl Acad Sci USA 110: E2677-86.
119. Reed SC, Lamason RL, Risca VI, Abernathy E, et al. 2014. Rickettsia actin-based motility occurs in distinct phases mediated by different actin nucleators. Curr Biol 24: 98-103.
120. Alvarez DE, Agaisse H. 2013. The formin FHOD1 and the small GTPase Rac1 promote vaccinia virus actin-based motility. J Cell Biol 202: 1075-90.