The cytoskeleton in cell-autonomous immunity: Structural determinants of host defence

Nature Reviews Immunology

Volumn 15, Issue 9, 2015, Pages 559-573

  Mostowy, Serge ^a   Shenoy, Avinash R ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; C TYPE LECTIN RECEPTOR; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; COLCHICINE; CRYOPYRIN; F ACTIN; INFLAMMASOME; PYRIN; SEPTIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VIMENTIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; AUTOPHAGOSOME; AUTOPHAGY; BACTERIAL INFECTION; CELL AUTONOMOUS IMMUNITY; CELL DEATH; CELL DIVISION; CELLULAR IMMUNITY; CYTOSKELETON; HOST CELL; HOST RESISTANCE; IMMUNE RESPONSE; INNATE IMMUNITY; INTERMEDIATE FILAMENT; MICROTUBULE; NONHUMAN; PATHOGENESIS; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM; ANIMAL; HUMAN; IMMUNOLOGY; VIRUS INFECTION;

ACTINS; ANIMALS; BACTERIAL INFECTIONS; CELL DEATH; CYTOSKELETON; HUMANS; IMMUNITY, INNATE; INFLAMMASOMES; INTERMEDIATE FILAMENTS; MICROTUBULES; SEPTINS; VIRUS DISEASES;

EID: 84940449432     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri3877     Document Type: Review

References (164)

1. Randow F., MacMicking J. D., & James L. C. Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science 340, 701-706 (2013
2. Pasparakis M., & Vandenabeele P. Necroptosis and its role in inflammation. Nature 517, 311-320 (2015
3. Sridharan H., & Upton J. W. Programmed necrosis in microbial pathogenesis. Trends Microbiol. 22, 199-207 (2014
4. Kawai T., & Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650 (2011
5. Yoneyama M., Onomoto K., Jogi M., Akaboshi T., & Fujita T. Viral RNA detection by RIG I like receptors. Curr. Opin. Immunol. 32C, 48-53 (2015
6. Philpott D. J., Sorbara M. T., Robertson S. J., Croitoru K., & Girardin S. E. NOD proteins: regulators of inflammation in health and disease. Nat. Rev. Immunol. 14, 9-23 (2014
7. von Moltke J., Ayres J. S., Kofoed E. M., Chavarría-Smith J., & Vance R. E. Recognition of bacteria by inflammasomes. Ann. Rev. Immunol. 31, 73-106 (2013
8. Schattgen S. A., & Fitzgerald K. A. The PYHIN protein family as mediators of host defenses. Immunol. Rev. 243, 109-118 (2011
9. Dambuza I. M., & Brown G. D. C type lectins in immunity: recent developments. Curr. Opin. Immunol. 32C, 21-27 (2014
10. Deretic V. Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors. Curr. Opin. Immunol. 24, 21-31 (2012
11. Stolz A., Ernst A., & Dikic I. Cargo recognition and trafficking in selective autophagy. Nat. Cell Biol. 16, 495-501 (2014
12. Bonizzi G., & Karin M. The two NF κB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25, 280-288 (2004
13. Arthur J. S. C., & Ley S. C. Mitogen-activated protein kinases in innate immunity. Nat. Rev. Immunol. 13, 679-692 (2013
14. Tamura T., Yanai H., Savitsky D., & Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Ann. Rev. Immunol. 26, 535-584 (2008
15. MacMicking J. D. Interferon-inducible effector mechanisms in cell-autonomous immunity. Nat. Rev. Immunol. 12, 367-382 (2012
16. Schneider W. M., Chevillotte M. D., & Rice C. M. Interferon-stimulated genes: a complex web of host defenses. Ann. Rev. Immunol. 32, 513-545 (2014
17. Eldridge M. J. G., & Shenoy A. R. Antimicrobial inflammasomes: unified signalling against diverse bacterial pathogens. Curr. Opin. Microbiol. 23, 32-41 (2015
18. Shi J., et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514, 187-192 (2014
19. Aachoui Y., et al. Caspase 11 protects against bacteria that escape the vacuole. Science 339, 975-978 (2013
20. Kayagaki N., et al. Non-canonical inflammasome activation targets caspase 11. Nature 479, 117-121 (2011
21. Rathinam V. A. K., et al. TRIF licenses caspase 11 dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 150, 606-619 (2012
22. Kayagaki N., et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341, 1246-1249 (2013
23. Hagar J. A., Powell D. A., Aachoui Y., Ernst R. K., & Miao E. A. Cytoplasmic LPS activates caspase 11: implications in TLR4 independent endotoxic shock. Science 341, 1250-1253 (2013
24. Aachoui Y., Sagulenko V., Miao E. A., & Stacey K. J. Inflammasome-mediated pyroptotic and apoptotic cell death, and defense against infection. Curr. Opin. Microbiol. 16, 319-326 (2013
25. Levine B., Mizushima N., & Virgin H. W. Autophagy in immunity and inflammation. Nature 469, 323-335 (2011
26. Pollard T. D., & Cooper J. A. Actin, a central player in cell shape and movement. Science 326, 1208-1212 (2009
27. Desai A., & Mitchison T. J. Microtubule polymerization dynamics. Ann. Rev. Cell Dev. Biol. 13, 83-117 (1997
28. Herrmann H., Strelkov S. V., Burkhard P., & Aebi U. Intermediate filaments: primary determinants of cell architecture and plasticity. J. Clin. Invest. 119, 1772-1783 (2009
29. Mostowy S., & Cossart P. Septins: the fourth component of the cytoskeleton. Nat. Rev. Mol. Cell Biol. 13, 183-194 (2012
30. Haglund C. M., & Welch M. D. Pathogens and polymers: microbe-host interactions illuminate the cytoskeleton. J. Cell Biol. 195, 7-17 (2011
31. Keestra A. M., et al. Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature 496, 233-237 (2013
32. Hardt W. D., Chen L. M., Schuebel K. E., Bustelo X. R., & Galán J. E. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815-826 (1998
33. Kufer T. A., Kremmer E., Adam A. C., Philpott D. J., & Sansonetti P. J. The pattern-recognition molecule Nod1 is localized at the plasma membrane at sites of bacterial interaction. Cell. Microbiol. 10, 477-486 (2008
34. Fukazawa A., et al. GEF H1 mediated control of NOD1 dependent NF κB activation by Shigella effectors. PLoS Pathog. 4, e1000228 (2008
35. Bielig H., et al. The cofilin phosphatase slingshot homolog 1 (SSH1) links NOD1 signaling to actin remodeling. PLoS Pathog. 10, e1004351 (2014
36. Bravo-Cordero J. J., Magalhaes M. A. O., Eddy R. J., Hodgson L., & Condeelis J. Functions of cofilin in cell locomotion and invasion. Nat. Rev. Mol. Cell Biol. 14, 405-415 (2013
37. Le Bourhis L., et al. Role of Nod1 in mucosal dendritic cells during Salmonella pathogenicity island 1 independent Salmonella enterica serovar Typhimurium infection. Infect. Immun. 77, 5203-5203 (2009
38. Eitel J., et al. β PIX and Rac1 GTPase mediate trafficking and negative regulation of NOD2. J. Immunol. 181, 2664-2671 (2008
39. Legrand-Poels S., et al. Modulation of Nod2 dependent NF κB signaling by the actin cytoskeleton. J. Cell Sci. 120, 1299-1310 (2007
40. Zhao Y., et al. Control of NOD2 and Rip2 dependent innate immune activation by GEF H1. Inflamm. Bowel Dis. 18, 603-612 (2012
41. Stevens C., et al. The intermediate filament protein, vimentin, is a regulator of NOD2 activity. Gut 62, 695-707 (2013
42. Dangl J. L., Horvath D. M., & Staskawicz B. J. Pivoting the plant immune system from dissection to deployment. Science 341, 746-751 (2013
43. Savic S., Dickie L. J., Battellino M., & McDermott M. F. Familial mediterranean fever and related periodic fever syndromes/autoinflammatory diseases. Curr. Opin. Rheum. 24, 103-112 (2012
44. Xu H., et al. Innate immune sensing of bacterial modifications of Rho GTPases by the pyrin inflammasome. Nature 513, 237-241 (2014
45. Gavrilin M. A., et al. Activation of the pyrin inflammasome by intracellular Burkholderia cenocepacia. J. Immunol. 188, 3469-3477 (2012
46. Clemens D. L., Lee B. Y., & Horwitz M. A. Francisella tularensis enters macrophages via a novel process involving pseudopod loops. Infect. Immun. 73, 5892-5902 (2005
47. Gavrilin M. A., et al. Pyrin critical to macrophage IL 1β response to Francisella challenge. J. Immunol. 182, 7982-7989 (2009
48. Waite A. L., et al. Pyrin and ASC co localize to cellular sites that are rich in polymerizing actin. Exp. Biol. Med. 234, 40-52 (2009
49. Gavrilin M. A., & Wewers M. D. Francisella recognition by inflammasomes: differences between mice and men. Front. Microbiol. 2, 11 (2011
50. Fernandes-Alnemri T., et al. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat. Immunol. 11, 385-393 (2010
51. Jones J. W., et al. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl Acad. Sci. USA 107, 9771-9776 (2010
52. Rathinam V. A. K., et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11, 395-402 (2010
53. Kim M. L., et al. Aberrant actin depolymerization triggers the pyrin inflammasome and autoinflammatory disease that is dependent on IL 18, not IL 1β. J. Exp. Med. 212, 927-938 (2015
54. Kile B. T., et al. Mutations in the cofilin partner Aip1/Wdr1 cause autoinflammatory disease and macrothrombocytopenia. Blood 110, 2371-2380 (2007
55. Muñoz-Planillo R., et al. K+ efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity 38, 1142-1153 (2013
56. Lamkanfi M., & Dixit V. M. Mechanisms and functions of inflammasomes. Cell 157, 1013-1022 (2014
57. Misawa T., et al. Microtubule-driven spatial arrangement of mitochondria promotes activation of the NLRP3 inflammasome. Nat. Immunol. 14, 454-460 (2013
58. Martinon F., Petrilli V., Mayor A., Tardivel A., & Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237-241 (2006
59. dos Santos G., et al. Vimentin regulates activation of the NLRP3 inflammasome. Nat. Commun. 6, 6574 (2015
60. Shenoy A. R., et al. GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science 336, 481-485 (2012
61. Mishra B. B., et al. Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL 1β. Nat. Immunol. 14, 52-60 (2013
62. Park S., et al. The mitochondrial antiviral protein MAVS associates with NLRP3 and regulates its inflammasome activity. J. Immunol. 191, 4358-4366 (2013
63. Subramanian N., Natarajan K., Clatworthy M. R., Wang Z., & Germain R. N. The adaptor MAVS promotes NLRP3 mitochondrial localization and inflammasome activation. Cell 153, 348-361 (2013
64. Rees F., Hui M., & Doherty M. Optimizing current treatment of gout. Nat. Rev. Rheumatol. 10, 271-283 (2014
65. Goldbach-Mansky R. Current status of understanding the pathogenesis and management of patients with NOMID/CINCA. Curr. Rheumatol. Rep. 13, 123-131 (2011
66. Strowig T., Henao-Mejia J., Elinav E., & Flavell R. Inflammasomes in health and disease. Nature 481, 278-286 (2012
67. Zhang J. G., et al. The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity 36, 646-657 (2012
68. Ahrens S., et al. F actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR 1, a receptor for dead cells. Immunity 36, 635-645 (2012
69. Sancho D., et al. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 458, 899-903 (2009
70. Hanc P., et al. Structure of the complex of F actin and DNGR 1, a C type lectin receptor involved in dendritic cell cross-presentation of dead cell-associated antigens. Immunity 42, 839-849 (2015
71. Zelenay S., et al. The dendritic cell receptor DNGR 1 controls endocytic handling of necrotic cell antigens to favor cross-priming of CTLs in virus-infected mice. J. Clin. Invest. 122, 1615-1627 (2012
72. Caudron F., & Barral Y. Septins and the lateral compartmentalization of eukaryotic membranes. Dev. Cell 16, 493-506 (2009
73. Tran Van Nhieu G., et al. Actin-based confinement of calcium responses during Shigella invasion. Nat. Commun. 4, 1567 (2013
74. Iborra S., et al. The DC receptor DNGR 1 mediates cross-priming of CTLs during vaccinia virus infection in mice. J. Clin. Invest. 122, 1628-1643 (2012
75. Sandiford S. L., et al. Cytoplasmic actin is an extracellular insect immune factor which is secreted upon immune challenge and mediates phagocytosis and direct killing of bacteria, and is a Plasmodium antagonist. PLoS Pathog. 11, e1004631 (2015
76. Aktories K., Lang A. E., Schwan C., & Mannherz H. G. Actin as target for modification by bacterial protein toxins. FEBS J. 278, 4526-4543 (2011
77. Goodridge H. S., Underhill D. M., & Touret N. Mechanisms of Fc receptor and dectin 1 activation for phagocytosis. Traffic 13, 1062-1071 (2012
78. Rosas M., et al. The induction of inflammation by dectin 1 in vivo is dependent on myeloid cell programming and the progression of phagocytosis. J. Immunol. 181, 3549-3557 (2008
79. Watts C., West M. A., & Zaru R. TLR signalling regulated antigen presentation in dendritic cells. Curr. Opin. Immunol. 22, 124-130 (2010
80. Underhill D. M., & Goodridge H. S. Information processing during phagocytosis. Nat. Rev. Immunol. 12, 492-502 (2012
81. Kagan J. C., et al. TRAM couples endocytosis of toll-like receptor 4 to the induction of interferon β. Nat. Immunol. 9, 361-368 (2008
82. Sasai M., Linehan M. M., & Iwasaki A. Bifurcation of toll-like receptor 9 signaling by adaptor protein 3. Science 329, 1530-1534 (2010
83. Gotoh K., et al. Selective control of type I IFN induction by the Rac activator DOCK2 during TLR-mediated plasmacytoid dendritic cell activation. J. Exp. Med. 207, 721-730 (2010
84. Parker D., & Prince A. Staphylococcus aureus induces type I IFN signaling in dendritic cells via TLR9. J. Immunol. 189, 4040-4046 (2012
85. Torchinsky M. B., Garaude J., Martin A. P., & Blander J. M. Innate immune recognition of infected apoptotic cells directs TH17 cell differentiation. Nature 458, 78-82 (2009
86. Kong L., et al. An essential role for RIG I in toll-like receptor-stimulated phagocytosis. Cell Host Microbe 6, 150-161 (2009
87. Mostowy S., et al. Septins regulate bacterial entry into host cells. PLoS ONE 4, e4196 (2009
88. Mostowy S., et al. Septin 11 restricts InlB-mediated invasion by Listeria. J. Biol. Chem. 284, 11613-11621 (2009
89. Huang Y. W., et al. Mammalian septins are required for phagosome formation. Mol. Biol. Cell 19, 1717-1726 (2008
90. Golebiewska U., et al. Evidence for a fence that impedes the diffusion of phosphatidylinositol 4,5 bisphosphate out of the forming phagosomes of macrophages. Mol. Biol. Cell 22, 3498-3507 (2011
91. Mizushima N., Yoshimori T., & Ohsumi Y. The role of Atg proteins in autophagosome formation. Ann. Rev. Cell Dev. Biol. 27, 107-132 (2011
92. Mostowy S., & Cossart P. Bacterial autophagy: restriction or promotion of bacterial replication?. Trends Cell Biol. 22, 283-291 (2012
93. Huang J., & Brumell J. H. Bacteria-autophagy interplay: a battle for survival. Nat. Rev. Micro. 12, 101-114 (2014
94. Mostowy S. Multiple roles of the cytoskeleton in bacterial autophagy. PLoS Pathog. 10, e1004409 (2014
95. Monastyrska I., Rieter E., Klionsky D. J., & Reggiori F. Multiple roles of the cytoskeleton in autophagy. Biol. Rev. 84, 431-448 (2009
96. Mostowy S., et al. Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microbe 8, 433-444 (2010
97. Mostowy S., et al. p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. J. Biol. Chem. 286, 26987-26995 (2011
98. Ogawa M., et al. Escape of intracellular Shigella from autophagy. Science 307, 727-731 (2005
99. Ogawa M., et al. A Tecpr1 dependent selective autophagy pathway targets bacterial pathogens. Cell Host Microbe 9, 376-389 (2011
100. Chen D., et al. A mammalian autophagosome maturation mechanism mediated by TECPR1 and the Atg12-Atg5 conjugate. Mol. Cell 45, 629-641 (2012
101. Yoshikawa Y., et al. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat. Cell Biol. 11, 1233-1240 (2009
102. Schroeder N., Mota L. J., & Méresse S. Salmonella-induced tubular networks. Trends Microbiol. 19, 268-277 (2011
103. Thurston T. L. M., Ryzhakov G., Bloor S., von Muhlinen N., & Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 10, 1215-1221 (2009
104. Zheng Y. T., et al. The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J. Immunol. 183, 5909-5916 (2009
105. Wild P., et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333, 228-233 (2011
106. Yu H. B., et al. Autophagy facilitates Salmonella replication in HeLa cells. mBio 5, e00865 14 (2014
107. Wang R. C., et al. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science 338, 956-959 (2012
108. Kumar Y., & Valdivia R. H. Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds. Cell Host Microbe 4, 159-169 (2008
109. Al Zeer M. A., Al Younes H. M., Lauster D., Abu Lubad M., & Meyer T. F. Autophagy restricts Chlamydia trachomatis growth in human macrophages via IFNG-inducible guanylate binding proteins. Autophagy 9, 50-62 (2012
110. Kim B. H., et al. A family of IFN γ-inducible 65 kD GTPases protects against bacterial infection. Science 332, 717-721 (2011
111. Ostler N., et al. Gamma interferon-induced guanylate binding protein 1 is a novel actin cytoskeleton remodeling factor. Mol. Cell. Biol. 34, 196-209 (2014
112. Tanaka-Takiguchi Y., Kinoshita M., & Takiguchi K. Septin-mediated uniform bracing of phospholipid membranes. Curr. Biol. 19, 140-145 (2009
113. Mostowy S., et al. The zebrafish as a new model for the in vivo study of Shigella flexneri interaction with phagocytes and bacterial autophagy. PLoS Pathog. 9, e1003588 (2013
114. Sanjuan M. A., et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257 (2007
115. West A. P., et al. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472, 476-480 (2011
116. Randow F., & Youle R. J. Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host Microbe 15, 403-411 (2014
117. Manzanillo P. S., et al. The ubiquitin ligase parkin mediates resistance to intracellular pathogens. Nature 501, 512-516 (2013
118. Li J., et al. Caspase 11 regulates cell migration by promoting Aip1-Cofilin-mediated actin depolymerization. Nat. Cell Biol. 9, 276-286 (2007
119. Li J., Yin H. L., & Yuan J. Flightless I regulates proinflammatory caspases by selectively modulating intracellular localization and caspase activity. J. Cell Biol. 181, 321-333 (2008
120. Man S. M., et al. Actin polymerization as a key innate immune effector mechanism to control Salmonella infection. Proc. Natl Acad. Sci. USA 111, 17588-17593 (2014
121. Jin J., et al. LRRFIP2 negatively regulates NLRP3 inflammasome activation in macrophages by promoting Flightless-I mediated caspase 1 inhibition. Nat. Commun. 4, 2075 (2013
122. Akhter A., et al. Caspase 11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization. Immunity 37, 35-47 (2012
123. Vance R. E. The NAIP/NLRC4 inflammasomes. Curr. Opin. Immunol. 32, 84-89 (2015
124. Ablasser A., et al. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503, 530-534 (2013
125. Cai X., Chiu Y. H., & Chen, Zhijian J. The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol. Cell 54, 289-296 (2014
126. McEwan W. A., et al. Intracellular antibody-bound pathogens stimulate immune signaling via the Fc receptor TRIM21. Nat. Immunol. 14, 327-336 (2013
127. Tam J. C. H., Bidgood S. R., McEwan W. A., & James L. C. Intracellular sensing of complement C3 activates cell autonomous immunity. Science 345, 1256070 (2014
128. Xia P., et al. Sox2 functions as a sequence-specific DNA sensor in neutrophils to initiate innate immunity against microbial infection. Nat. Immunol. 16, 366-375 (2015
129. Knodler L. A., et al. Noncanonical inflammasome activation of caspase 4/caspase 11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe 16, 249-256 (2014
130. Ma Y., Galluzzi L., Zitvogel L., & Kroemer G. Autophagy and cellular immune responses. Immunity 39, 211-227 (2013
131. Snider N. T., & Omary M. B. Post-translational modifications of intermediate filament proteins: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 15, 163-177 (2014
132. Terman J. R., & Kashina A. Post-translational modification and regulation of actin. Curr. Opin. Cell Biol. 25, 30-38 (2013
133. Song Y., & Brady S. T. Post-translational modifications of tubulin: pathways to functional diversity of microtubules. Trends Cell Biol. 25, 125-136 (2014
134. Swanson J. A. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 9, 639-649 (2008
135. Cameron L. A., Robbins J. R., Footer M. J., & Theriot J. A. Biophysical parameters influence actin based movement, trajectory, and initiation in a cell-free system. Mol. Biol. Cell 15, 2312-2323 (2004
136. Cabeen M. T., & Jacobs-Wagner C. The bacterial cytoskeleton. Ann. Rev. Genet. 44, 365-392 (2010
137. Jones L. J. F., Carballido-López R., & Errington J. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104, 913-922 (2001
138. Bi E., & Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161-164 (1991
139. Ausmees N., Kuhn J. R., & Jacobs-Wagner C. The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115, 705-713 (2003
140. Weirich C. S., Erzberger J. P., & Barral Y. The septin family of GTPases: architecture and dynamics. Nat. Rev. Mol. Cell Biol. 9, 478-489 (2008
141. Ghosal D., Trambaiolo D., Amos L. A., & Löwe J. MinCD cell division proteins form alternating copolymeric cytomotive filaments. Nat. Commun. 5, 5341 (2014
142. Angus K. L., & Griffiths G. M. Cell polarisation and the immunological synapse. Curr. Opin. Cell Biol. 25, 85-91 (2013
143. Harwood N. E., & Batista F. D. The cytoskeleton coordinates the early events of B cell activation. Cold Spring Harb. Perspect. Biol. 3, a002360 (2011
144. Thrasher A. J., & Burns S. O. WASP: a key immunological multitasker. Nat. Rev. Immunol. 10, 182-192 (2010
145. Frade A. F., et al. Polymorphism in the α cardiac muscle actin 1 gene is associated to susceptibility to chronic inflammatory cardiomyopathy. PLoS ONE 8, e83446 (2013
146. Solomon J. P., Page L. J., Balch W. E., & Kelly J. W. Gelsolin amyloidosis: genetics, biochemistry, pathology and possible strategies for therapeutic intervention. Crit. Rev. Biochem. Mol. Biol. 47, 282-296 (2012
147. Kuhlenbaumer G., et al. Mutations in SEPT9 cause hereditary neuralgic amyotrophy. Nat. Genet. 37, 1044-1046 (2005
148. Blanchoin L., Boujemaa-Paterski R., Sykes C., & Plastino J. Actin dynamics, architecture, and mechanics in cell motility. Physiol. Rev. 94, 235-263 (2014
149. Hyams J. S., & Lloyd C. W. Microtubules (eds Hyams J. S., & Lloyd C. W.) (Wiley-Liss, 1994
150. Saarikangas J., & Barral Y. The emerging functions of septins in metazoans. EMBO Rep. 12, 1118-1126 (2011
151. Cossart P., & Sansonetti P. J. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242-248 (2004
152. Pizarro-Cerdá J., Kühbacher A., & Cossart P. Entry of Listeria monocytogenes in mammalian epithelial cells: an updated view. Cold Spring Harb. Perspect. Med. 2, a010009 (2012
153. Carayol N., & Tran Van Nhieu G. Tips and tricks about Shigella invasion of epithelial cells. Curr. Opin. Microbiol. 16, 32-37 (2013
154. Caron E., et al. Subversion of actin dynamics by EPEC and EHEC. Curr. Opin. Microbiol. 9, 40-45 (2006
155. Jaffe A. B., & Hall A. RHO GTPases: biochemistry and biology. Ann. Rev. Cell Dev. Biol. 21, 247-269 (2005
156. Aktories K. Bacterial protein toxins that modify host regulatory GTPases. Nat. Rev. Micro. 9, 487-498 (2011
157. Welch M. D., & Way M. Arp2/3 mediated actin-based motility: a tail of pathogen abuse. Cell Host Microbe 14, 242-255 (2013
158. Reed S. C. O., Lamason R. L., Risca V. I., Abernathy E., & Welch M. D. Rickettsia actin-based motility occurs in distinct phases mediated by different actin nucleators. Curr. Biol. 24, 98-103 (2014
159. Benanti E. L., Nguyen C. M., & Welch M. D. Virulent Burkholderia species mimic host actin polymerases to drive actin-based motility. Cell 161, 348-360 (2015
160. Asrat S., de Jesús D. A., Hempstead A. D., Ramabhadran V., & Isberg R. R. Bacterial pathogen manipulation of host membrane trafficking. Ann. Rev. Cell Dev. Biol. 30, 79-109 (2014
161. Kokes M., et al. Integrating chemical mutagenesis and whole-genome sequencing as a platform for forward and reverse genetic analysis of Chlamydia. Cell Host Microbe 17, 716-725 (2015
162. Rubinsztein D. C., Bento C. F., & Deretic V. Therapeutic targeting of autophagy in neurodegenerative and infectious diseases. J. Exp. Med. 212, 979-990 (2015
163. Mackeh R., Perdiz D., Lorin S., Codogno P., & Poüs C. Autophagy and microtubules -new story, old players. J. Cell Sci. 126, 1071-1080 (2013
164. Dobbs K., et al. Inherited DOCK2 deficiency in patients with early-onset invasive infections. N. Engl. J. Med. 372, 2409-2422 (2015