Impact of dynasore an inhibitor of dynamin II on Shigella flexneri infection

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Lum, Mabel ^a   Attridge, Stephen R ^a   Morona, Renato ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN II; DYNASORE; ENZYME INHIBITOR; F ACTIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL EYE INFECTION; BACTERIAL VIRULENCE; CELL PROTECTION; CONTROLLED STUDY; DISEASE COURSE; DRUG PROTEIN BINDING; ENZYME INHIBITION; EYE INFLAMMATION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFECTION CONTROL; MALE; MOUSE; MOUSE MODEL; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SHIGELLA FLEXNERI; SHIGELLOSIS; WEIGHT REDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CELL DEATH; CONGO RED; DYNAMIN II; DYSENTERY, BACILLARY; ESCHERICHIA COLI K12; EYE; HELA CELLS; HUMANS; HYDRAZONES; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED BALB C; MICROSCOPY, FLUORESCENCE;

EID: 84893157028     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084975     Document Type: Article

References (70)

1. Bardhan P, Faruque ASG, Naheed A, DA S (2010) Decrease in Shigellosis-related deaths without Shigella spp.-specific interventions. Asia - Emerg Infect Dis 16: 1718-1723. doi:10.3201/eid1611.090934.
2. Barry EM, Pasetti MF, Sztein MB, Fasano A, Kotloff KL et al. (2013) Progress and pitfalls in Shigella vaccine research. Nat Rev Gastroenterol Hepatol 10: 245-255. doi:10.1038/nrgastro.2013.12. PubMed: 23419287.
3. Yang F, Yang J, Zhang X, Chen L, Jiang Y et al. (2005) Genome dynamics and diversity of Shigella species, the etiologic agents of bacillary dysentery. Nucleic Acids Res 33: 6445-6458. doi:10.1093/nar/gki954. PubMed: 16275786.
4. Zychlinsky A, Prevost MC, Sansonetti PJ (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167-169. doi:10.1038/358167a0. PubMed: 1614548.
5. Sansonetti PJ, Phalipon A, Arondel J, Thirumalai K, Banerjee S et al. (2000) Caspase-1 activation of IL-1beta and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12: 581-590. doi:10.1016/S1074-7613(00) 80209-5. PubMed: 10843390.
6. Sansonetti PJ, Ryter A, Clerc P, Maurelli AT, Mounier J (1986) Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect Immun 51: 461-469. PubMed: 3510976.
7. Cossart P, Sansonetti PJ (2004) Bacterial Invasion: The Paradigms of Enteroinvasive Pathogens. Science 304: 242-248. doi:10.1126/science.1090124. PubMed: 15073367.
8. Schuch R, Sandlin RC, Maurelli AT (1999) A system for identifying post-invasion functions of invasion genes: requirements for the Mxi-Spa type III secretion pathway of Shigella flexneri in intercellular dissemination. Mol Microbiol 34: 675-689. doi:10.1046/j.1365-2958.1999.01627.x. PubMed: 10564508.
9. Makino S, Sasakawa C, Kamata K, Kurata T, Yoshikawa M (1986) A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri 2a. Cell 46: 551-555. doi:10.1016/0092-8674(86)90880-9. PubMed: 3524856.
10. Lett MC, Sasakawa C, Okada N, Sakai T, Makino S et al. (1989) virG, a plasmid-coded virulence gene of Shigella flexneri: identification of the virG protein and determination of the complete coding sequence. J Bacteriol 171: 353-359. PubMed: 2644195.
11. Bernardini ML, Mounier J, d'Hauteville H, Coquis-Rondon M, Sansonetti PJ (1989) Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc Natl Acad Sci U S A 86: 3867-3871. doi:10.1073/pnas.86.10.3867. PubMed: 2542950.
12. Kotloff KL, Noriega F, Losonsky GA, Sztein MB, Wasserman SS et al. (1996) Safety, immunogenicity, and transmissibility in humans of CVD 1203, a live oral Shigella flexneri 2a vaccine candidate attenuated by deletions in aroA and virG. Infect Immun 64: 4542-4548. PubMed: 8890204.
13. Sansonetti PJ, Arondel J, Huerre M, Harada A, Matsushima K (1999) Interleukin-8 Controls Bacterial Transepithelial Translocation at the Cost of Epithelial Destruction in Experimental Shigellosis. Infect Immun 67: 1471-1480. PubMed: 10024597.
14. Hong M, Payne SM (1997) Effect of mutations in Shigella flexneri chromosomal and plasmid-encoded lipopolysaccharide genes on invasion and serum resistance. Mol Microbiol 24: 779-791. doi:10.1046/j.1365-2958.1997.3731744.x. PubMed: 9194705.
15. Okamura N, Nagai T, Nakaya R, Kondo S, Murakami M et al. (1983) HeLa cell invasiveness and O antigen of Shigella flexneri as separate and prerequisite attributes of virulence to evoke keratoconjunctivitis in guinea pigs. Infect Immun 39: 505-513. PubMed: 6187681.
16. Miyoshi J, Takai Y (2005) Molecular perspective on tight-junction assembly and epithelial polarity. Adv Drug Deliv Rev 57: 815-855. doi:10.1016/j.addr.2005.01.008. PubMed: 15820555.
17. Rajabian T, Gavicherla B, Heisig M, Müller-Altrock S, Goebel W et al. (2009) The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-to-cell spread of Listeria. Nat Cell Biol 11: 1212-1218. doi:10.1038/ncb1964. PubMed: 19767742.
18. Sansonetti PJ, Mounier J, Prévost MC, Mège RM (1994) Cadherin expression is required for the spread of Shigella flexneri between epithelial cells. Cell 76: 829-839. doi:10.1016/0092-8674(94)90358-1. PubMed: 8124719.
19. 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: 3463-3471. PubMed: 1910001.
20. Bishai EA, Sidhu GS, Li W, Dhillon J, Bohil AB et al. (2013) Myosin-X Facilitates Shigella-induced Membrane Protrusions and Cell-to-Cell Spread. Cell Microbiol, 15: 353-367. PubMed: 23083060.
21. Tran Van Nhieu G, Clair C, Bruzzone R, Mesnil M, Sansonetti P et al. (2003) Connexin-dependent inter-cellular communication increases invasion and dissemination of Shigella in epithelial cells. Nat Cell Biol 5: 720-726. doi:10.1038/ncb1021. PubMed: 12844145.
22. Heindl JE, Saran I, Yi C-r, Lesser CF, Goldberg MB (2010) Requirement for formin-induced actin polymerization during spread of Shigella. Infect Immun, 78: 193-203. PubMed: 19841078.
23. Esue O, Harris ES, Higgs HN, Wirtz D (2008) The Filamentous Actin Cross-Linking/Bundling Activity of Mammalian Formins. J Mol Biol 384: 324-334. doi:10.1016/j.jmb.2008.09.043. PubMed: 18835565.
24. Fukumatsu M, Ogawa M, Arakawa S, Suzuki M, Nakayama K et al. (2012) Shigella Targets Epithelial Tricellular Junctions and Uses a Noncanonical Clathrin-Dependent Endocytic Pathway to Spread Between Cells. Cell Host Microbe 11: 325-336. doi:10.1016/j.chom.2012.03.001. PubMed: 22520461.
25. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12: 517-533. doi:10.1038/nrg3048. PubMed: 21779028.
26. Muhlberg AB, Warnock DE, Schmid SL (1997) Domain structure and intramolecular regulation of dynamin GTPase. EMBO J 16: 6676-6683. doi:10.1093/emboj/16.22.6676. PubMed: 9362482.
27. Kessels MM, Engqvist-Goldstein AEY, Drubin DG, Qualmann B (2001) Mammalian Abp1, a Signal-responsive F-Actin-binding Protein, Links the Actin Cytoskeleton to Endocytosis Via the GTPase Dynamin. J Cell Biol 153: 351-366. doi:10.1083/jcb.153.2.351. PubMed: 11309416.
28. McNiven MA, Kim L, Krueger EW, Orth JD, Cao H et al. (2000) Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151: 187-198. doi:10.1083/jcb.151.1.187. PubMed: 11018064.
29. Burger KNJ, Demel RA, Schmid SL, de Kruijff B (2000) Dynamin Is Membrane-Active: Lipid Insertion Is Induced by Phosphoinositides and Phosphatidic Acid. Biochimie 39: 12485-12493. doi:10.1021/bi000971r. PubMed: 11015230.
30. Cao H, Garcia F, McNiven MA (1998) Differential distribution of dynamin isoforms in mammalian cells. Mol Biol Cell 9: 2595-2609. doi:10.1091/mbc.9.9. 2595. PubMed: 9725914.
31. Chappie JS, Acharya S, Leonard M, Schmid SL, Dyda F (2010) G domain dimerization controls dynamin's assembly-stimulated GTPase activity. Nature 465: 435-440. doi:10.1038/nature09032. PubMed: 20428113.
32. Faelber K, Posor Y, Gao S, Held M, Roske Y et al. (2011) Crystal structure of nucleotide-free dynamin. Nature 477: 556-560. doi:10.1038/ nature10369. PubMed: 21927000.
33. Ford MGJ, Jenni S, Nunnari J (2011) The crystal structure of dynamin. Nature 477: 561-566. doi:10.1038/nature10441. PubMed: 21927001.
34. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C et al. (2006) Dynasore, a Cell-Permeable Inhibitor of Dynamin. Dev Cell 10: 839-850. doi:10.1016/j.devcel.2006.04.002. PubMed: 16740485.
35. Terada N, Ohno N, Saitoh S, Saitoh Y, Fujii Y et al. (2009) Involvement of dynamin-2 in formation of discoid vesicles in urinary bladder umbrella cells. Cell Tissue Res 337: 91-102. PubMed: 19479281.
36. Chen C-L, Hou W-H, Liu I-H, Hsiao G, Huang SS et al. (2009) Inhibitors of clathrin-dependent endocytosis enhance TGFβ signaling and responses. J Cell Sci 122: 1863-1871. doi:10.1242/jcs.038729. PubMed: 19461075.
37. Gao D, Zhang L, Dhillon R, Hong T-T, Shaw RM et al. (2013) Dynasore Protects Mitochondria and Improves Cardiac Lusitropy in Langendorff Perfused Mouse. Heart - PLOS ONE 8: e60967. doi:10.1371/journal.pone.0060967.
38. Morona R, Daniels C, Van Den Bosch L (2003) Genetic modulation of Shigella flexneri 2a lipopolysaccharide O antigen modal chain length reveals that it has been optimized for virulence. Microbiology 149: 925-939. doi:10.1099/mic.0.26141-0. PubMed: 12686635.
39. Lagendijk EL, Validov S, Lamers GEM, De Weert S, Bloemberg GV (2010) Genetic tools for tagging Gram-negative bacteria with mCherry for visualization in vitro and in natural habitats, biofilm and pathogenicity studies. FEMS Microbiol Lett 305: 81-90. doi:10.1111/j.1574-6968.2010.01916.x. PubMed: 20180857.
40. Baker SJ, Gunn JS, Morona R (1999) The Salmonella typhi melittin resistance gene pqaB affects intracellular growth in PMA-differentiated U937 cells, polymyxin B resistance and lipopolysaccharide. Microbiology 145 (2): 367-378. doi:10.1099/13500872-145-2-367. PubMed: 10075419.
41. Morona R, van den Bosch L, Manning PA (1995) Molecular, genetic, and topological characterization of O-antigen chain length regulation in Shigella flexneri. J Bacteriol 177: 1059-1068. PubMed: 7532168.
42. May KL, Morona R (2008) Mutagenesis of the Shigella flexneri autotransporter IcsA reveals novel functional regions involved in IcsA biogenesis and recruitment of host neural Wiscott-Aldrich syndrome protein. J Bacteriol 190: 4666-4676. doi:10.1128/JB.00093-08. PubMed: 18456802.
43. Qualmann B, Kelly RB (2000) Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J Cell Biol 148: 1047-1062. doi:10.1083/jcb.148.5.1047. PubMed: 10704453.
44. Oaks EV, Wingfield ME, Formal SB (1985) Plaque formation by virulent Shigella flexneri. Infect Immun 48: 124-129. PubMed: 3884506.
45. Murayama SY, Sakai T, Makino S, Kurata T, Sasakawa C et al. (1986) The use of mice in the Sereny test as a virulence assay of Shigellae and enteroinvasive Escherichia coli. Infect Immun 51: 696-698. PubMed: 3510985.
46. Ambrosi C, Pompili M, Scribano D, Zagaglia C, Ripa S et al. (2012) Outer membrane protein A (OmpA): a new player in Shigella flexneri protrusion formation and inter-cellular spreading. PLOS ONE 7: e49625. doi:10.1371/journal. pone.0049625. PubMed: 23166731.
47. Prunier A-L, Schuch R, Fernández RE, Mumy KL, Kohler H et al. (2007) nadA and nadB of Shigella flexneri 5a are antivirulence loci responsible for the synthesis of quinolinate, a small molecule inhibitor of Shigella pathogenicity. Microbiology 153: 2363-2372. doi:10.1099/mic.0.2007/006916-0. PubMed: 17600080.
48. Egile C, d'Hauteville H, Parsot C, Sansonetti PJ (1997) SopA, the outer membrane protease responsible for polar localization of IcsA in Shigella flexneri. Mol Microbiol 23: 1063-1073. doi:10.1046/j.1365-2958.1997.2871652.x. PubMed: 9076742.
49. Sandlin RC, Goldberg MB, Maurelli AT (1996) Effect of O side-chain length and composition on the virulence of Shigella flexneri 2a. Mol Microbiol 22: 63-73. doi:10.1111/j.1365-2958.1996.tb02656.x. PubMed: 8899709.
50. Goldberg MB, Bârzu O, Parsot C, Sansonetti PJ (1993) Unipolar localization and ATPase activity of IcsA, a Shigella flexneri protein involved in intracellular movement. J Bacteriol 175: 2189-2196. PubMed: 8468279.
51. Suzuki T, Miki H, Takenawa T, Sasakawa C (1998) Neural Wiskott-Aldrich syndrome protein is implicated in the actin-based motility of Shigella flexneri. EMBO J 17: 2767-2776. doi:10.1093/emboj/17.10.2767. PubMed: 9582270.
52. Goldberg MB (2001) Actin-Based Motility of Intracellular Microbial Pathogens. Microbiol Mol Biol Rev 65: 595-626. doi:10.1128/MMBR.65.4.595-626. 2001. PubMed: 11729265.
53. Sandlin RC, Lampel KA, Keasler SP, Goldberg MB, Stolzer AL et al. (1995) Avirulence of rough mutants of Shigella flexneri: requirement of O antigen for correct unipolar localization of IcsA in the bacterial outer membrane. Infect Immun 63: 229-237. PubMed: 7528731.
54. Van den Bosch L, Manning PA, Morona R (1997) Regulation of O-antigen chain length is required for Shigella flexneri virulence. Mol Microbiol 23: 765-775. doi:10.1046/j.1365-2958.1997.2541625.x. PubMed: 9157247.
55. Suzuki T, Mimuro H, Suetsugu S, Miki H, Takenawa T et al. (2002) Neural Wiskott-Aldrich syndrome protein (N-WASP) is the specific ligand for Shigella VirG among the WASP family and determines the host cell type allowing actin-based spreading. Cell Microbiol 4: 223-233. doi:10.1046/j.1462-5822.2002. 00185.x. PubMed: 11952639.
56. Buchrieser C, Glaser P, Rusniok C, Nedjari H, D'Hauteville H et al. (2000) The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol Microbiol 38: 760-771. doi:10.1046/j.1365-2958.2000.02179.x. PubMed: 11115111.
57. Suzuki T, Yoshikawa Y, Ashida H, Iwai H, Toyotome T et al. (2006) High vaccine efficacy against shigellosis of recombinant noninvasive Shigella mutant that expresses Yersinia invasin. J Immunol 177: 4709-4717. PubMed: 16982910.
58. Lee E, De Camilli P (2002) Dynamin at actin tails. Proc Natl Acad Sci U S A 99: 161-166. doi:10.1073/pnas.012607799. PubMed: 11782545.
59. Moreau V, Frischknecht F, Reckmann I, Vincentelli R, Rabut G et al. (2000) A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nat Cell Biol 2: 441-448. doi:10.1038/35017080. PubMed: 10878810.
60. Shin N, Ahn N, Chang-Ileto B, Park J, Takei K et al. (2008) SNX9 regulates tubular invagination of the plasma membrane through interaction with actin cytoskeleton and dynamin 2. J Cell Sci 121: 1252-1263. doi:10.1242/jcs.016709. PubMed: 18388313.
61. Ashida H, Ogawa M, Mimuro H, Kobayashi T, Sanada T et al. (2011) Shigella are versatile mucosal pathogens that circumvent the host innate immune system. Curr Opin Immunol 23: 448-455. doi:10.1016/j.coi.2011.06.001. PubMed: 21763117.
62. Shim DH, Suzuki T, Chang SY, Park SM, Sansonetti PJ et al. (2007) New animal model of shigellosis in the Guinea pig: its usefulness for protective efficacy studies. J Immunol 178: 2476-2482. PubMed: 17277155.
63. Jeong KI, Zhang Q, Nunnari J, Tzipori S (2010) A piglet model of acute gastroenteritis induced by Shigella dysenteriae Type 1. J Infect Dis 201: 903-911. doi:10.1086/650995. PubMed: 20136414.
64. Yang J-Y, Lee S-N, Chang S-Y, Ko H-J, Ryu S et al. (2013) A Mouse Model of Shigellosis by Intraperitoneal. Infection - J Infect Dis.
65. Rabbani GH, Albert MJ, Rahman H, Islam M, Mahalanabis D et al. (1995) Development of an improved animal model of shigellosis in the adult rabbit by colonic infection with Shigella flexneri 2a. Infect Immun 63: 4350-4357. PubMed: 7591070.
66. Barman S, Saha DR, Ramamurthy T, Koley H (2011) Development of a new guinea-pig model of shigellosis. FEMS Immunol Med Microbiol 62: 304-314. doi:10.1111/j.1574-695X.2011.00810.x. PubMed: 21539623.
67. Senerovic L, Tsunoda SP, Goosmann C, Brinkmann V, Zychlinsky A et al. (2012) Spontaneous formation of IpaB ion channels in host cell membranes reveals how Shigella induces pyroptosis in macrophages. Cell Death. Drosophila Inf Service 3: e384.
68. Abrusci P, Vergara-Irigaray M, Johnson S, Beeby MD, Hendrixson DR et al. (2013) Architecture of the major component of the type III secretion system export apparatus. Nat Struct Mol Biol 20: 99-104. PubMed: 23222644.
69. Smirnova E, Shurland D-L, Ryazantsev SN, van der Bliek AM (1998) A Human Dynamin-related Protein Controls the Distribution of Mitochondria. J Cell Biol 143: 351-358. doi:10.1083/jcb.143.2.351. PubMed: 9786947.
70. Francis MS, Thomas CJ (1996) Effect of multiplicity of infection on Listeria monocytogenes pathogenicity for HeLa and Caco-2 cell lines. J Med Microbiol 45: 323-330. doi:10.1099/00222615-45-5-323. PubMed: 8918946.