IQGAP1 in microbial pathogenesis: Targeting the actin cytoskeleton

FEBS Letters

Volumn 585, Issue 5, 2011, Pages 723-729

  Kim, Hugh ^a   White, Colin D ^b   Sacks, David B ^c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

EPEC; IQGAP1; Microbial pathogenesis; Salmonella

Indexed keywords

GUANOSINE TRIPHOSPHATASE; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN CDC42; RAC1 PROTEIN;

ACTIN POLYMERIZATION; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL INVASION; CELLULAR DISTRIBUTION; CYTOSKELETON; DOWN REGULATION; ESCHERICHIA COLI; HOST PATHOGEN INTERACTION; HUMAN; INFECTION; INTERNALIZATION; MICROTUBULE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEOMICS; SALMONELLA TYPHIMURIUM; TYPE III SECRETION SYSTEM; VIRUS ENTRY; VIRUS PATHOGENESIS; VIRUS REPLICATION;

BACTERIA (MICROORGANISMS); SALMONELLA;

EID: 79952317707     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.01.041     Document Type: Review

References (85)

1. D.G. Nyachuba Foodborne illness: is it on the rise? Nutr. Rev. 68 2010 257 269
2. S. Gruenheid, and B.B. Finlay Microbial pathogenesis and cytoskeletal function Nature 422 2003 775 781 (Pubitemid 36514121)
3. J.T. Barbieri, M.J. Riese, and K. Aktories Bacterial toxins that modify the actin cytoskeleton Annu. Rev. Cell Dev. Biol. 18 2002 315 344 (Pubitemid 35387354)
4. K. Rottner, T.E. Stradal, and J. Wehland Bacteria-host-cell interactions at the plasma membrane: stories on actin cytoskeleton subversion Dev. Cell 9 2005 3 17 (Pubitemid 40903655)
5. M.W. Briggs, and D.B. Sacks IQGAP proteins are integral components of cytoskeletal regulation EMBO Rep. 4 2003 571 574 (Pubitemid 36939947)
6. M.D. Brown, and D.B. Sacks IQGAP1 in cellular signaling: bridging the GAP Trends Cell Biol. 16 2006 242 249 (Pubitemid 43744436)
7. C.D. White, M.D. Brown, and D.B. Sacks IQGAPs in cancer: a family of scaffold proteins underlying tumorigenesis FEBS Lett. 583 2009 1817 1824
8. S.C. Mateer, A.E. McDaniel, V. Nicolas, G.M. Habermacher, M.J. Lin, D.A. Cromer, M.E. King, and G.S. Bloom The mechanism for regulation of the F-actin binding activity of IQGAP1 by calcium/calmodulin J. Biol. Chem. 277 2002 12324 12333 (Pubitemid 34952803)
9. J.W. Erickson, R.A. Cerione, and M.J. Hart Identification of an actin cytoskeletal complex that includes IQGAP and the Cdc42 GTPase J. Biol. Chem. 272 1997 24443 24447 (Pubitemid 27418652)
10. M. Fukata Regulation of cross-linking of actin filament by IQGAP1, a target for Cdc42 J. Biol. Chem. 272 1997 29579 29583
11. M.J. Hart, M.G. Callow, B. Souza, and P. Polakis IQGAP1, a calmodulin-binding protein with a RasGAP-related domain, is a potential effector for Cdc42Hs EMBO J. 15 1996 2997 3005 (Pubitemid 26187748)
12. L.B. Bensenor, H.M. Kan, N. Wang, H. Wallrabe, L.A. Davidson, Y. Cai, D.A. Schafer, and G.S. Bloom IQGAP1 regulates cell motility by linking growth factor signaling to actin assembly J. Cell Sci. 120 2007 658 669 (Pubitemid 46437900)
13. J.M. Swart-Mataraza, Z. Li, and D.B. Sacks IQGAP1 is a component of Cdc42 signaling to the cytoskeleton J. Biol. Chem. 277 2002 24753 24763 (Pubitemid 34952007)
14. J. Noritake, T. Watanabe, K. Sato, S. Wang, and K. Kaibuchi IQGAP1: a key regulator of adhesion and migration J. Cell Sci. 118 2005 2085 2092 (Pubitemid 40872832)
15. D.T. Brandt, and R. Grosse Get to grips: steering local actin dynamics with IQGAPs EMBO Rep. 8 2007 1019 1023 (Pubitemid 350042336)
16. J.A. McGarvey, D. Wagner, and L.E. Bermudez Differential gene expression in mononuclear phagocytes infected with pathogenic and non-pathogenic mycobacteria Clin. Exp. Immunol. 136 2004 490 500 (Pubitemid 38703683)
17. J.V. Rogers, Y.W. Choi, L.F. Giannunzio, P.J. Sabourin, D.M. Bornman, E.G. Blosser, and C.L. Sabourin Transcriptional responses in spleens from mice exposed to Yersinia pestis CO92 Microb. Pathog. 43 2007 67 77 (Pubitemid 46991193)
18. D.T. Brandt, S. Marion, G. Griffiths, T. Watanabe, K. Kaibuchi, and R. Grosse Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation J. Cell Biol. 178 2007 193 200 (Pubitemid 47076456)
19. J.C. Patel, and J.E. Galan Manipulation of the host actin cytoskeleton by Salmonella - all in the name of entry Curr. Opin. Microbiol. 8 2005 10 15 (Pubitemid 40203220)
20. M.D. Brown, L. Bry, Z. Li, and D.B. Sacks Actin pedestal formation by enteropathogenic Escherichia coli is regulated by IQGAP1, calcium, and calmodulin J. Biol. Chem. 283 2008 35212 35222
21. C. Buss, D. Muller, C. Ruter, G. Heusipp, and M.A. Schmidt Identification and characterization of Ibe, a novel type III effector protein of A/E pathogens targeting human IQGAP1 Cell. Microbiol. 11 2009 661 677
22. L.M. McLaughlin The Salmonella SPI2 effector SseI mediates long-term systemic infection by modulating host cell migration PLoS Pathog. 5 2009 e1000671
23. B. Coburn, I. Sekirov, and B.B. Finlay Type III secretion systems and disease Clin. Microbiol. Rev. 20 2007 535 549 (Pubitemid 47623767)
24. S. Etienne-Manneville, and A. Hall Rho GTPases in cell biology Nature 420 2002 629 635 (Pubitemid 36764489)
25. R.D. Hayward, and V. Koronakis Direct modulation of the host cell cytoskeleton by Salmonella actin-binding proteins Trends Cell Biol. 12 2002 15 20 (Pubitemid 34164152)
26. M.D. Brown, L. Bry, Z. Li, and D.B. Sacks IQGAP1 regulates Salmonella invasion through interactions with actin, Rac1, and Cdc42 J. Biol. Chem. 282 2007 30265 30272 (Pubitemid 350035299)
27. J.M. Mataraza, Z. Li, H.W. Jeong, M.D. Brown, and D.B. Sacks Multiple proteins mediate IQGAP1-stimulated cell migration Cell. Signal. 19 2007 1857 1865 (Pubitemid 47081378)
28. J. Sun Pathogenic bacterial proteins and their anti-inflammatory effects in the eukaryotic host Anti-Inflamm. Anti-Allergy Agents Med. Chem. 8 2009 214 227
29. M.A. Gordon Salmonella infections in immunocompromised adults J. Infect. 56 2008 413 422
30. F. Geissmann, M.G. Manz, S. Jung, M.H. Sieweke, M. Merad, and K. Ley Development of monocytes, macrophages, and dendritic cells Science 327 2010 656 661
31. L.R. Prost, S. Sanowar, and S.I. Miller Salmonella sensing of anti-microbial mechanisms to promote survival within macrophages Immunol. Rev. 219 2007 55 65 (Pubitemid 47390009)
32. C. Cheminay, A. Mohlenbrink, and M. Hensel Intracellular Salmonella inhibit antigen presentation by dendritic cells J. Immunol. 174 2005 2892 2899 (Pubitemid 40279707)
33. K.G. Campellone Cytoskeleton-modulating effectors of enteropathogenic and enterohaemorrhagic Escherichia coli: Tir, EspFU and actin pedestal assembly FEBS J. 277 2010 2390 2402
34. C.R. Yi, and M.B. Goldberg Enterohemorrhagic Escherichia coli raises the I-BAR Proc. Natl. Acad. Sci. USA 106 2009 6431 6432
35. G. Frankel, and A.D. Phillips Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal Cell. Microbiol. 10 2008 549 556 (Pubitemid 351194084)
36. E. Caron, V.F. Crepin, N. Simpson, S. Knutton, J. Garmendia, and G. Frankel Subversion of actin dynamics by EPEC and EHEC Curr. Opin. Microbiol. 9 2006 40 45 (Pubitemid 43184336)
37. D. Chin, and A.R. Means Calmodulin: a prototypical calcium sensor Trends Cell Biol. 10 2000 322 328 (Pubitemid 30445239)
38. J. Lee, A. Ishihara, G. Oxford, B. Johnson, and K. Jacobson Regulation of cell movement is mediated by stretch-activated calcium channels Nature 400 1999 382 386 (Pubitemid 29344206)
39. T.J. Baldwin, W. Ward, A. Aitken, S. Knutton, and P.H. Williams Elevation of intracellular free calcium levels in HEp-2 cells infected with enteropathogenic Escherichia coli Infect. Immun. 59 1991 1599 1604
40. 2+ of type III secretion of diffusely adhering enteropathogenic Escherichia coli Infect. Immun. 71 2003 1725 1732 (Pubitemid 36368700)
41. J.L. Joyal, R.S. Annan, Y.D. Ho, M.E. Huddleston, S.A. Carr, M.J. Hart, and D.B. Sacks Calmodulin modulates the interaction between IQGAP1 and Cdc42. Identification of IQGAP1 by nanoelectrospray tandem mass spectrometry J. Biol. Chem. 272 1997 15419 15425 (Pubitemid 27255567)
42. D.L. Goosney, D.G. Knoechel, and B.B. Finlay Enteropathogenic E. coli, Salmonella, and Shigella: masters of host cell cytoskeletal exploitation Emerg. Infect. Dis. 5 1999 216 223 (Pubitemid 29200619)
43. D.R. Bridge, M.J. Novotny, E.R. Moore, and J.C. Olson Role of host cell polarity and leading edge properties in Pseudomonas type III secretion Microbiology 156 2010 356 373
44. V.S. Conlin, S.B. Curtis, Y. Zhao, E.D. Moore, V.C. Smith, R.M. Meloche, B.B. Finlay, and A.M. Buchan Helicobacter pylori infection targets adherens junction regulatory proteins and results in increased rates of migration in human gastric epithelial cells Infect. Immun. 72 2004 5181 5192 (Pubitemid 39223404)
45. I. Mohr Phosphorylation and dephosphorylation events that regulate viral mRNA translation Virus Res. 119 2006 89 99 (Pubitemid 43786256)
46. A. Ono, D. Demirov, and E.O. Freed Relationship between human immunodeficiency virus type 1 Gag multimerization and membrane binding J. Virol. 74 2000 5142 5150 (Pubitemid 30313854)
47. X. Yuan, X. Yu, T.H. Lee, and M. Essex Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor J. Virol. 67 1993 6387 6394 (Pubitemid 23309102)
48. J. Leung, A. Yueh, F.S. Appah Jr., B. Yuan, K. de los Santos, and S.P. Goff Interaction of Moloney murine leukemia virus matrix protein with IQGAP EMBO J. 25 2006 2155 2166
49. T. Golub, and P. Caroni PI(4, 5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility J. Cell Biol. 169 2005 151 165 (Pubitemid 40562922)
50. M. Fukata Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170 Cell 109 2002 873 885 (Pubitemid 34786002)
51. M. Roy, Z. Li, and D.B. Sacks IQGAP1 is a scaffold for mitogen-activated protein kinase signaling Mol. Cell. Biol. 25 2005 7940 7952 (Pubitemid 41262989)
52. J.G. Ren, Z. Li, and D.B. Sacks IQGAP1 modulates activation of B-Raf Proc. Natl. Acad. Sci. USA 104 2007 10465 10469 (Pubitemid 47185688)
53. M. Roy, Z. Li, and D.B. Sacks IQGAP1 binds ERK2 and modulates its activity J. Biol. Chem. 279 2004 17329 17337 (Pubitemid 38560493)
54. P. Tang, C.L. Sutherland, M.R. Gold, and B.B. Finlay Listeria monocytogenes invasion of epithelial cells requires the MEK1/ERK2 mitogen-activated protein kinase pathway Infect. Immun. 66 1998 1106 1112 (Pubitemid 28101153)
55. A. Aiastui, M.G. Pucciarelli, and F. Garcia-del Portillo Salmonella enterica serovar typhimurium invades fibroblasts by multiple routes differing from the entry into epithelial cells Infect. Immun. 78 2010 2700 2713
56. O. Steele-Mortimer The Salmonella-containing vacuole: moving with the times Curr. Opin. Microbiol. 11 2008 38 45
57. J.H. Brumell, and S. Grinstein Role of lipid-mediated signal transduction in bacterial internalization Cell. Microbiol. 5 2003 287 297 (Pubitemid 37009907)
58. D. Drecktrah, L.A. Knodler, and O. Steele-Mortimer Modulation and utilization of host cell phosphoinositides by Salmonella Infect. Immun. 72 2004 4331 4335 (Pubitemid 38989288)
59. M.A. Reddy, N.V. Prasadarao, C.A. Wass, and K.S. Kim Phosphatidylinositol 3-kinase activation and interaction with focal adhesion kinase in Escherichia coli K1 invasion of human brain microvascular endothelial cells J. Biol. Chem. 275 2000 36769 36774 (Pubitemid 32002085)
60. K. Ireton, B. Payrastre, H. Chap, W. Ogawa, H. Sakaue, M. Kasuga, and P. Cossart A role for phosphoinositide 3-kinase in bacterial invasion Science 274 1996 780 782 (Pubitemid 26398257)
61. A.S. Sechi, and J. Wehland The actin cytoskeleton and plasma membrane connection: PtdIns(4, 5)P2 influences cytoskeletal protein activity at the plasma membrane J. Cell Sci. 113 2000 3685 3695
62. M.R. Terebiznik Elimination of host cell PtdIns(4, 5)P2 by bacterial SigD promotes membrane fission during invasion by Salmonella Nat. Cell Biol. 4 2002 766 773 (Pubitemid 35214770)
63. G.G. Gundersen Evolutionary conservation of microtubule-capture mechanisms Nat. Rev. Mol. Cell Biol. 3 2002 296 304 (Pubitemid 34619265)
64. T.A. Oelschlaeger, P. Guerry, and D.J. Kopecko Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii Proc. Natl. Acad. Sci. USA 90 1993 6884 6888 (Pubitemid 23207318)
65. M. Kuhn The microtubule depolymerizing drugs nocodazole and colchicine inhibit the uptake of Listeria monocytogenes by P388D1 macrophages FEMS Microbiol. Lett. 160 1998 87 90 (Pubitemid 28098556)
66. B.K. Dhakal, and M.A. Mulvey Uropathogenic Escherichia coli invades host cells via an HDAC6-modulated microtubule-dependent pathway J. Biol. Chem. 284 2009 446 454
67. S. Yoshida, and C. Sasakawa Exploiting host microtubule dynamics: a new aspect of bacterial invasion Trends Microbiol. 11 2003 139 143 (Pubitemid 36332134)
68. S.A. Wickstrom Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae Dev. Cell 19 2010 574 588
69. A.K. Pullikuth, and A.D. Catling Scaffold mediated regulation of MAPK signaling and cytoskeletal dynamics: a perspective Cell. Signal. 19 2007 1621 1632 (Pubitemid 46935436)
70. W. Kolch Coordinating ERK/MAPK signalling through scaffolds and inhibitors Nat. Rev. Mol. Cell Biol. 6 2005 827 837 (Pubitemid 41568732)
71. K.J. Procyk, P. Kovarik, A. von Gabain, and M. Baccarini Salmonella typhimurium and lipopolysaccharide stimulate extracellularly regulated kinase activation in macrophages by a mechanism involving phosphatidylinositol 3-kinase and phospholipase D as novel intermediates Infect. Immun. 67 1999 1011 1017 (Pubitemid 29108471)
72. B.K. Coombes, and J.B. Mahony Identification of MEK- and phosphoinositide 3-kinase-dependent signalling as essential events during Chlamydia pneumoniae invasion of HEp2 cells Cell. Microbiol. 4 2002 447 460 (Pubitemid 34835659)
73. D.J. Evans, I.A. Maltseva, J. Wu, and S.M. Fleiszig Pseudomonas aeruginosa internalization by corneal epithelial cells involves MEK and ERK signal transduction proteins FEMS Microbiol. Lett. 213 2002 73 79 (Pubitemid 34804520)
74. 2+/calmodulin and Cdc42 signaling J. Biol. Chem. 274 1999 464 470 (Pubitemid 29035084)
75. B. Hu, B. Shi, M.J. Jarzynka, J.J. Yiin, C. D'Souza-Schorey, and S.Y. Cheng ADP ribosylation factor 6 regulates glioma cell invasion through the IQ-domain GTPase-activating protein 1-Rac1-mediated pathway Cancer Res. 69 2009 794 801
76. R.D. Meyer, D.B. Sacks, and N. Rahimi IQGAP1-dependent signaling pathway regulates endothelial cell proliferation and angiogenesis PLoS ONE 3 2008 e3848
77. 2+/calmodulin-dependent protein kinase II J. Cell. Physiol. 208 2006 213 219 (Pubitemid 43849007)
78. L.Y. Bourguignon, E. Gilad, K. Rothman, and K. Peyrollier Hyaluronan-CD44 interaction with IQGAP1 promotes Cdc42 and ERK signaling leading to actin binding, Elk-1/estrogen receptor transcriptional activation and ovarian cancer progression J. Biol. Chem. 280 2005 11961 11972 (Pubitemid 40418513)
79. phox translocation and reactive oxygen species generation in lung endothelial cells J. Biol. Chem. 284 2009 15339 15352
80. E.N. Rittmeyer, S. Daniel, S.C. Hsu, and M.A. Osman A dual role for IQGAP1 in regulating exocytosis J. Cell Sci. 121 2008 391 403 (Pubitemid 351356710)
81. C. Le Clainche IQGAP1 stimulates actin assembly through the N-WASP-Arp2/3 pathway J. Biol. Chem. 282 2007 426 435 (Pubitemid 47076652)
82. J.M. Mataraza, M.W. Briggs, Z. Li, R. Frank, and D.B. Sacks Identification and characterization of the Cdc42 binding site of IQGAP1 Biochem. Biophys. Res. Commun. 305 2003 315 321 (Pubitemid 36555470)
83. S. Kuroda, M. Fukata, K. Kobayashi, M. Nakafuku, N. Nomura, A. Iwamatsu, and K. Kaibuchi Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1 J. Biol. Chem. 271 1996 23363 23367 (Pubitemid 26314782)
84. M.J. Smith The PTB domain of ShcA couples receptor activation to the cytoskeletal regulator IQGAP1 EMBO J. 29 2010 884 896
85. K. Takahashi, and K. Suzuki Requirement of kinesin-mediated membrane transport of WAVE2 along microtubules for lamellipodia formation promoted by hepatocyte growth factor Exp. Cell Res. 314 2008 2313 2322