Listeria monocytogenes internalin B activates junctional endocytosis to accelerate intestinal invasion

PLoS Pathogens

Volumn 6, Issue 5, 2010, Pages 1-15

  Pentecost, Mickey ^a   Kumaran, Jyothi ^b   Ghosh, Partho ^b   Amieva, Manuel R ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DYNAMIN; INTERNALIN A; INTERNALIN B; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; INLB PROTEIN, LISTERIA MONOCYTOGENES; MEMBRANE PROTEIN; PROTEIN TYROSINE KINASE; RON PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; CONTROLLED STUDY; ENDOCYTOSIS; FEMALE; IN VIVO STUDY; INTERNALIZATION; INTESTINE INFECTION; INTESTINE VILLUS; KIDNEY CELL; LISTERIA MONOCYTOGENES; MOUSE; NONHUMAN; PROTEIN FUNCTION; ANIMAL; BAGG ALBINO MOUSE; CELL JUNCTION; CELL LINE; CELL POLARITY; CYTOLOGY; DOG; EPITHELIUM CELL; KIDNEY; LISTERIOSIS; METABOLISM; MICROBIOLOGY; MICROVILLUS; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; MURINAE; MUS;

ANIMALS; BACTERIAL PROTEINS; CADHERINS; CELL LINE; CELL POLARITY; DOGS; DYNAMINS; ENDOCYTOSIS; EPITHELIAL CELLS; FEMALE; INTERCELLULAR JUNCTIONS; KIDNEY; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICROVILLI; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 77954040534     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000900     Document Type: Article

References (135)

1. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
2. Dramsi S, Biswas I, Maguin E, Braun L, Mastroeni P, et al. (1995) Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol 16: 251-261.
3. Gaillard JL, Berche P, Frehel C, Gouin E, Cossart P (1991) Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 65: 1127-1141.
4. Temm-Grove CJ, Jockusch BM, Rohde M, Niebuhr K, Chakraborty T, et al. (1994) Exploitation of microfilament proteins by Listeria monocytogenes: microvillus-like composition of the comet tails and vectorial spreading in polarized epithelial sheets. J Cell Sci 107 (Pt 10): 2951-2960.
5. Ray K, Marteyn B, Sansonetti PJ, Tang CM (2009) Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat Rev Microbiol 7: 333-340.
6. Lecuit M, Vandormael-Pournin S, Lefort J, Huerre M, Gounon P, et al. (2001) A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292: 1722-1725.
7. Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84: 923-932.
8. Schubert WD, Urbanke C, Ziehm T, Beier V, Machner MP, et al. (2002) Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell 111: 825-836.
9. Lecuit M, Dramsi S, Gottardi C, Fedor-Chaiken M, Gumbiner B, et al. (1999) A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. Embo J 18: 3956-3963.
10. Shen Y, Naujokas M, Park M, Ireton K (2000) InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103: 501-510.
11. Li N, Xiang GS, Dokainish H, Ireton K, Elferink LA (2005) The listeria protein internalin B mimics hepatocyte growth factor-induced receptor trafficking. Traffic 6: 459-473.
12. Greiffenberg L, Goebel W, Kim KS, Weiglein I, Bubert A, et al. (1998) Interaction of Listeria monocytogenes with human brain microvascular endothelial cells: InlB-dependent invasion, long-term intracellular growth, and spread from macrophages to endothelial cells. Infect Immun 66: 5260-5267.
13. Lingnau A, Domann E, Hudel M, Bock M, Nichterlein T, et al. (1995) Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfAdependent and -independent mechanisms. Infect Immun 63: 3896-3903.
14. Parida SK, Domann E, Rohde M, Muller S, Darji A, et al. (1998) Internalin B is essential for adhesion and mediates the invasion of Listeria monocytogenes into human endothelial cells. Mol Microbiol 28: 81-93.
15. Banerjee M, Copp J, Vuga D, Marino M, Chapman T, et al. (2004) GW domains of the Listeria monocytogenes invasion protein InlB are required for potentiation of Met activation. Mol Microbiol 52: 257-271.
16. Marino M, Banerjee M, Jonquieres R, Cossart P, Ghosh P (2002) GW domains of the Listeria monocytogenes invasion protein InlB are SH3-like and mediate binding to host ligands. Embo J 21: 5623-5634.
17. Copp J, Marino M, Banerjee M, Ghosh P, van der Geer P (2003) Multiple regions of internalin B contribute to its ability to turn on the Ras-mitogenactivated protein kinase pathway. J Biol Chem 278: 7783-7789.
18. Marino M, Braun L, Cossart P, Ghosh P (1999) Structure of the lnlB leucinerich repeats, a domain that triggers host cell invasion by the bacterial pathogen L. monocytogenes. Mol Cell 4: 1063-1072.
19. Ireton K, Payrastre B, Cossart P (1999) The Listeria monocytogenes protein InlB is an agonist of mammalian phosphoinositide 3-kinase. J Biol Chem 274: 17025-17032.
20. Disson O, Grayo S, Huillet E, Nikitas G, Langa-Vives F, et al. (2008) Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature 455: 1114-1118.
21. Niemann HH, Jager V, Butler PJ, van den Heuvel J, Schmidt S, et al. (2007) Structure of the human receptor tyrosine kinase met in complex with the Listeria invasion protein InlB. Cell 130: 235-246.
22. Gaillard JL, Jaubert F, Berche P (1996) The inlAB locus mediates the entry of Listeria monocytogenes into hepatocytes in vivo. J Exp Med 183: 359-369.
23. Dramsi S, Bourdichon F, Cabanes D, Lecuit M, Fsihi H, et al. (2004) FbpA, a novel multifunctional Listeria monocytogenes virulence factor. Mol Microbiol 53: 639-649.
24. Khelef N, Lecuit M, Bierne H, Cossart P (2006) Species specificity of the Listeria monocytogenes InlB protein. Cell Microbiol 8: 457-470.
25. Bakardjiev AI, Stacy BA, Fisher SJ, Portnoy DA (2004) Listeriosis in the pregnant guinea pig: a model of vertical transmission. Infect Immun 72: 489-497.
26. Robbins JR, Skrzypczynska KM, Zeldovich VB, Kapidzic M, Bakardjiev AI (2010) Placental syncytiotrophoblast constitutes a major barrier to vertical transmission of Listeria monocytogenes. PLoS Pathog 6: e1000732.
27. Bonazzi M, Veiga E, Pizarro-Cerda J, Cossart P (2008) Successive posttranslational modifications of E-cadherin are required for InlA-mediated internalization of Listeria monocytogenes. Cell Microbiol 10: 2208-2222.
28. Sousa S, Cabanes D, Bougneres L, Lecuit M, Sansonetti P, et al. (2007) Src, cortactin and Arp2/3 complex are required for E-cadherin-mediated internalization of Listeria into cells. Cell Microbiol 9: 2629-2643.
29. Bergmann B, Raffelsbauer D, Kuhn M, Goetz M, Hom S, et al. (2002) InlAbut not InlB-mediated internalization of Listeria monocytogenes by nonphagocytic mammalian cells needs the support of other internalins. Mol Microbiol 43: 557-570.
30. Pentecost M, Otto G, Theriot JA, Amieva MR (2006) Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog 2: e3.
31. Crepaldi T, Pollack AL, Prat M, Zborek A, Mostov K, et al. (1994) Targeting of the SF/HGF receptor to the basolateral domain of polarized epithelial cells. J Cell Biol 125: 313-320.
32. Cossart P (1998) Interactions of the bacterial pathogen Listeria monocytogenes with mammalian cells: bacterial factors, cellular ligands, and signaling. Folia Microbiol (Praha) 43: 291-303.
33. Boller K, Vestweber D, Kemler R (1985) Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epithelial cells. J Cell Biol 100: 327-332.
34. Potten CS, Loeffler M (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110: 1001-1020.
35. Madara JL (1990) Maintenance of the macromolecular barrier at cell extrusion sites in intestinal epithelium: physiological rearrangement of tight junctions. J Membr Biol 116: 177-184.
36. Gordon JI, Hermiston ML (1994) Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr Opin Cell Biol 6: 795-803.
37. Corfe BM, Dive C, Garrod DR (2000) Changes in intercellular junctions during apoptosis precede nuclear condensation or phosphatidylserine exposure on the cell surface. Cell Death Differ 7: 234-235.
38. Rosenblatt J, Raff MC, Cramer LP (2001) An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 11: 1847-1857.
39. Sue D, Fink D, Wiedmann M, Boor KJ (2004) sigmaB-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 150: 3843-3855.
40. McGann P, Wiedmann M, Boor KJ (2007) The alternative sigma factor sigma B and the virulence gene regulator PrfA both regulate transcription of Listeria monocytogenes internalins. Appl Environ Microbiol 73: 2919-2930.
41. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
42. Sleator RD, Watson D, Hill C, Gahan CG (2009) The interaction between Listeria monocytogenes and the host gastrointestinal tract. Microbiology 155: 2463-2475.
43. Pamer EG (2004) Immune responses to Listeria monocytogenes. Nat Rev Immunol 4: 812-823.
44. Wollert T, Pasche B, Rochon M, Deppenmeier S, van den Heuvel J, et al. (2007) Extending the host range of Listeria monocytogenes by rational protein design. Cell 129: 891-902.
45. Wollert T, Heinz DW, Schubert WD (2007) Thermodynamically reengineering the listerial invasion complex InlA/E-cadherin. Proc Natl Acad Sci U S A 104: 13960-13965.
46. Kamei T, Matozaki T, Sakisaka T, Kodama A, Yokoyama S, et al. (1999) Coendocytosis of cadherin and c-Met coupled to disruption of cell-cell adhesion in MDCK cells-regulation by Rho, Rac and Rab small G proteins. Oncogene 18: 6776-6784.
47. Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HE, et al. (2002) Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat Cell Biol 4: 222-231.
48. Robbins JR, Barth AI, Marquis H, de Hostos EL, Nelson WJ, et al. (1999) Listeria monocytogenes exploits normal host cell processes to spread from cell to cell. J Cell Biol 146: 1333-1350.
49. Lecuit M, Sonnenburg JL, Cossart P, Gordon JI (2007) Functional genomic studies of the intestinal response to a foodborne enteropathogen in a humanized gnotobiotic mouse model. J Biol Chem 282: 15065-15072.
50. Racz P, Tenner K, Mero E (1972) Experimental Listeria enteritis. I. An electron microscopic study of the epithelial phase in experimental listeria infection. Lab Invest 26: 694-700.
51. Tilney LG, Portnoy DA (1989) Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 109: 1597-1608.
52. Jonquieres R, Bierne H, Fiedler F, Gounon P, Cossart P (1999) Interaction between the protein InlB of Listeria monocytogenes and lipoteichoic acid: a novel mechanism of protein association at the surface of gram-positive bacteria. Mol Microbiol 34: 902-914.
53. Jonquieres R, Pizarro-Cerda J, Cossart P (2001) Synergy between the N- and C-terminal domains of InlB for efficient invasion of non-phagocytic cells by Listeria monocytogenes. Mol Microbiol 42: 955-965.
54. Braun L, Nato F, Payrastre B, Mazie JC, Cossart P (1999) The 213-amino-acid leucine-rich repeat region of the listeria monocytogenes InlB protein is sufficient for entry into mammalian cells, stimulation of PI 3-kinase and membrane ruffling. Mol Microbiol 34: 10-23.
55. Veiga E, Guttman JA, Bonazzi M, Boucrot E, Toledo-Arana A, et al. (2007) Invasive and adherent bacterial pathogens co-Opt host clathrin for infection. Cell Host Microbe 2: 340-351.
56. Seveau S, Tham TN, Payrastre B, Hoppe AD, Swanson JA, et al. (2007) A FRET analysis to unravel the role of cholesterol in Rac1 and PI 3-kinase activation in the InlB/Met signalling pathway. Cell Microbiol 9: 790-803.
57. Bierne H, Gouin E, Roux P, Caroni P, Yin HL, et al. (2001) A role for cofilin and LIM kinase in Listeria-induced phagocytosis. J Cell Biol 155: 101-112.
58. Seveau S, Bierne H, Giroux S, Prevost MC, Cossart P (2004) Role of lipid rafts in E-cadherin-and HGF-R/Met-mediated entry of Listeria monocytogenes into host cells. J Cell Biol 166: 743-753.
59. Veiga E, Cossart P (2005) Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nat Cell Biol.
60. Bierne H, Miki H, Innocenti M, Scita G, Gertler FB, et al. (2005) WASPrelated proteins, Abi1 and Ena/VASP are required for Listeria invasion induced by the Met receptor. J Cell Sci 118: 1537-1547.
61. Braun L, Ohayon H, Cossart P (1998) The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol Microbiol 27: 1077-1087.
62. Cossart P, Pizarro-Cerda J, Lecuit M (2003) Invasion of mammalian cells by Listeria monocytogenes: functional mimicry to subvert cellular functions. Trends Cell Biol 13: 23-31.
63. Ireton K (2007) Entry of the bacterial pathogen Listeria monocytogenes into mammalian cells. Cell Microbiol 9: 1365-1375.
64. Goetz M, Bubert A, Wang G, Chico-Calero I, Vazquez-Boland JA, et al. (2001) Microinjection and growth of bacteria in the cytosol of mammalian host cells. Proc Natl Acad Sci U S A 98: 12221-12226.
65. Gregory SH, Sagnimeni AJ, Wing EJ (1997) Internalin B promotes the replication of Listeria monocytogenes in mouse hepatocytes. Infect Immun 65: 5137-5141.
66. Balkovetz DF, Pollack AL, Mostov KE (1997) Hepatocyte growth factor alters the polarity of Madin-Darby canine kidney cell monolayers. J Biol Chem 272: 3471-3477.
67. Wang X, Le P, Liang C, Chan J, Kiewlich D, et al. (2003) Potent and selective inhibitors of the Met [hepatocyte growth factor/scatter factor (HGF/SF) receptor] tyrosine kinase block HGF/SF-induced tumor cell growth and invasion. Mol Cancer Ther 2: 1085-1092.
68. Bierne H, Cossart P (2002) InlB, a surface protein of Listeria monocytogenes that behaves as an invasin and a growth factor. J Cell Sci 115: 3357-3367.
69. Karunasagar I, Senghaas B, Krohne G, Goebel W (1994) Ultrastructural study of Listeria monocytogenes entry into cultured human colonic epithelial cells. Infect Immun 62: 3554-3558.
70. Hartsock A, Nelson WJ (2008) Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778: 660-669.
71. Izumi G, Sakisaka T, Baba T, Tanaka S, Morimoto K, et al. (2004) Endocytosis of E-cadherin regulated by Rac and Cdc42 small G proteins through IQGAP1 and actin filaments. J Cell Biol 166: 237-248.
72. Bryant DM, Kerr MC, Hammond LA, Joseph SR, Mostov KE, et al. (2007) EGF induces macropinocytosis and SNX1-modulated recycling of E-cadherin. J Cell Sci 120: 1818-1828.
73. Pizarro-Cerda J, Payrastre B, Wang YJ, Veiga E, Yin HL, et al. (2007) Type II phosphatidylinositol 4-kinases promote Listeria monocytogenes entry into target cells. Cell Microbiol 9: 2381-2390.
74. 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.
75. Guttman JA, Finlay BB (2009) Tight junctions as targets of infectious agents. Biochim Biophys Acta 1788: 832-841.
76. Vogelmann R, Amieva MR, Falkow S, Nelson WJ (2004) Breaking into the epithelial apical-junctional complex-news from pathogen hackers. Curr Opin Cell Biol 16: 86-93.
77. Sousa S, Lecuit M, Cossart P (2005) Microbial strategies to target, cross or disrupt epithelia. Curr Opin Cell Biol.
78. O'Hara JR, Buret AG (2008) Mechanisms of intestinal tight junctional disruption during infection. Front Biosci 13: 7008-7021.
79. Hauck CR, Agerer F, Muenzner P, Schmitter T (2006) Cellular adhesion molecules as targets for bacterial infection. Eur J Cell Biol 85: 235-242.
80. Coyne CB, Shen L, Turner JR, Bergelson JM (2007) Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2: 181-192.
81. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, et al. (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275: 1320-1323.
82. Antar AA, Konopka JL, Campbell JA, Henry RA, Perdigoto AL, et al. (2009) Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell Host Microbe 5: 59-71.
83. Barton ES, Forrest JC, Connolly JL, Chappell JD, Liu Y, et al. (2001) Junction adhesion molecule is a receptor for reovirus. Cell 104: 441-451.
84. Liu S, Yang W, Shen L, Turner JR, Coyne CB, et al. (2009) Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection. J Virol 83: 2011-2014.
85. Yang W, Qiu C, Biswas N, Jin J, Watkins SC, et al. (2008) Correlation of the tight junction-like distribution of Claudin-1 to the cellular tropism of hepatitis C virus. J Biol Chem 283: 8643-8653.
86. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, et al. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446: 801-805.
87. Yoon M, Spear PG (2002) Disruption of adherens junctions liberates nectin-1 to serve as receptor for herpes simplex virus and pseudorabies virus entry. J Virol 76: 7203-7208.
88. Spear PG (2004) Herpes simplex virus: receptors and ligands for cell entry. Cell Microbiol 6: 401-410.
89. Graham KL, Halasz P, Tan Y, Hewish MJ, Takada Y, et al. (2003) Integrinusing rotaviruses bind alpha2beta1 integrin alpha2 I domain via VP4 DGE sequence and recognize alphaXbeta2 and alphaVbeta3 by using VP7 during cell entry. J Virol 77: 9969-9978.
90. Ciarlet M, Crawford SE, Cheng E, Blutt SE, Rice DA, et al. (2002) VLA-2 (alpha2beta1) integrin promotes rotavirus entry into cells but is not necessary for rotavirus attachment. J Virol 76: 1109-1123.
91. Guerrero CA, Mendez E, Zarate S, Isa P, Lopez S, et al. (2000) Integrin alpha(v)beta(3) mediates rotavirus cell entry. Proc Natl Acad Sci U S A 97: 14644-14649.
92. Hewish MJ, Takada Y, Coulson BS (2000) Integrins alpha2beta1 and alpha4beta1 can mediate SA11 rotavirus attachment and entry into cells. J Virol 74: 228-236.
93. Clark MA, Hirst BH, Jepson MA (1998) M-cell surface beta1 integrin expression and invasin-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer's patch M cells. Infect Immun 66: 1237-1243.
94. Watarai M, Funato S, Sasakawa C (1996) Interaction of Ipa proteins of Shigella flexneri with alpha5beta1 integrin promotes entry of the bacteria into mammalian cells. J Exp Med 183: 991-999.
95. Isberg RR, Leong JM (1990) Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60: 861-871.
96. Taylor JM, Lin E, Susmarski N, Yoon M, Zago A, et al. (2007) Alternative entry receptors for herpes simplex virus and their roles in disease. Cell Host Microbe 2: 19-28.
97. Kopp SJ, Banisadr G, Glajch K, Maurer UE, Grunewald K, et al. (2009) Infection of neurons and encephalitis after intracranial inoculation of herpes simplex virus requires the entry receptor nectin-1. Proc Natl Acad Sci U S A.
98. Pincus Z, Theriot JA (2007) Comparison of quantitative methods for cell-shape analysis. J Microsc 227: 140-156.
99. Le TL, Yap AS, Stow JL (1999) Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J Cell Biol 146: 219-232.
100. Jarrett O, Stow JL, Yap AS, Key B (2002) Dynamin-dependent endocytosis is necessary for convergent-extension movements in Xenopus animal cap explants. Int J Dev Biol 46: 467-473.
101. Shaye DD, Casanova J, Llimargas M (2008) Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea. Nat Cell Biol 10: 964-970.
102. de Beco S, Gueudry C, Amblard F, Coscoy S (2009) Endocytosis is required for E-cadherin redistribution at mature adherens junctions. Proc Natl Acad Sci U S A.
103. Troyanovsky RB, Sokolov EP, Troyanovsky SM (2006) Endocytosis of cadherin from intracellular junctions is the driving force for cadherin adhesive dimer disassembly. Mol Biol Cell 17: 3484-3493.
104. Georgiou M, Marinari E, Burden J, Baum B (2008) Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr Biol 18: 1631-1638.
105. Paterson AD, Parton RG, Ferguson C, Stow JL, Yap AS (2003) Characterization of E-cadherin endocytosis in isolated MCF-7 and chinese hamster ovary cells: the initial fate of unbound E-cadherin. J Biol Chem 278: 21050-21057.
106. Seveau S, Pizarro-Cerda J, Cossart P (2007) Molecular mechanisms exploited by Listeria monocytogenes during host cell invasion. Microbes Infect 9: 1167-1175.
107. Pizarro-Cerda J, Cossart P (2006) Subversion of cellular functions by Listeria monocytogenes. J Pathol 208: 215-223.
108. Liu NQ, Lossinsky AS, Popik W, Li X, Gujuluva C, et al. (2002) Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen-activated protein kinase signaling pathway. J Virol 76: 6689-6700.
109. Amstutz B, Gastaldelli M, Kalin S, Imelli N, Boucke K, et al. (2008) Subversion of CtBP1-controlled macropinocytosis by human adenovirus serotype 3. Embo J 27: 956-969.
110. Raghu H, Sharma-Walia N, Veettil MV, Sadagopan S, Chandran B (2009) Kaposi's sarcoma-associated herpesvirus utilizes an actin polymerizationdependent macropinocytic pathway to enter human dermal microvascular endothelial and human umbilical vein endothelial cells. J Virol 83: 4895-4911.
111. Meier O, Boucke K, Hammer SV, Keller S, Stidwill RP, et al. (2002) Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J Cell Biol 158: 1119-1131.
112. Zenni MK, Giardina PC, Harvey HA, Shao J, Ketterer MR, et al. (2000) Macropinocytosis as a mechanism of entry into primary human urethral epithelial cells by Neisseria gonorrhoeae. Infect Immun 68: 1696-1699.
113. Watarai M, Makino S, Fujii Y, Okamoto K, Shirahata T (2002) Modulation of Brucella-induced macropinocytosis by lipid rafts mediates intracellular replication. Cell Microbiol 4: 341-355.
114. Watarai M, Derre I, Kirby J, Growney JD, Dietrich WF, et al. (2001) Legionella pneumophila is internalized by a macropinocytotic uptake pathway controlled by the Dot/Icm system and the mouse Lgn1 locus. J Exp Med 194: 1081-1096.
115. Gruenheid S, Finlay BB (2003) Microbial pathogenesis and cytoskeletal function. Nature 422: 775-781.
116. Finlay BB, Fry J, Rock EP, Falkow S (1989) Passage of Salmonella through polarized epithelial cells: role of the host and bacterium. J Cell Sci Suppl 11: 99-107.
117. Finlay BB, Ruschkowski S, Dedhar S (1991) Cytoskeletal rearrangements accompanying salmonella entry into epithelial cells. J Cell Sci 99 (Pt 2): 283-296.
118. Francis CL, Starnbach MN, Falkow S (1992) Morphological and cytoskeletal changes in epithelial cells occur immediately upon interaction with Salmonella typhimurium grown under low-oxygen conditions. Mol Microbiol 6: 3077-3087.
119. Dehio C, Prevost MC, Sansonetti PJ (1995) Invasion of epithelial cells by Shigella flexneri induces tyrosine phosphorylation of cortactin by a pp60c-srcmediated signalling pathway. Embo J 14: 2471-2482.
120. Garcia-Perez BE, Mondragon-Flores R, Luna-Herrera J (2003) Internalization of Mycobacterium tuberculosis by macropinocytosis in non-phagocytic cells. Microb Pathog 35: 49-55.
121. Garcia-Perez BE, Hernandez-Gonzalez JC, Garcia-Nieto S, Luna-Herrera J (2008) Internalization of a non-pathogenic mycobacteria by macropinocytosis in human alveolar epithelial A549 cells. Microb Pathog 45: 1-6.
122. Ginocchio CC, Olmsted SB, Wells CL, Galan JE (1994) Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76: 717-724.
123. Ketterer MR, Shao JQ, Hornick DB, Buscher B, Bandi VK, et al. (1999) Infection of primary human bronchial epithelial cells by Haemophilus influenzae: macropinocytosis as a mechanism of airway epithelial cell entry. Infect Immun 67: 4161-4170.
124. Bonazzi M, Spano S, Turacchio G, Cericola C, Valente C, et al. (2005) CtBP3/BARS drives membrane fission in dynamin-independent transport pathways. Nat Cell Biol 7: 570-580.
125. Swanson JA, Watts C (1995) Macropinocytosis. Trends Cell Biol 5: 424-428.
126. Saffarian S, Cocucci E, Kirchhausen T (2009) Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 7: e1000191.
127. Cureton DK, Massol RH, Saffarian S, Kirchhausen TL, Whelan SP (2009) Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog 5: e1000394.
128. Veiga E, Cossart P (2007) Listeria InlB takes a different route to met. Cell 130: 218-219.
129. Palacios F, Schweitzer JK, Boshans RL, D'Souza-Schorey C (2002) ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat Cell Biol 4: 929-936.
130. Shen A, Higgins DE (2005) The 59 untranslated region-mediated enhancement of intracellular listeriolysin O production is required for Listeria monocytogenes pathogenicity. Mol Microbiol 57: 1460-1473.
131. Lauer P, Chow MY, Loessner MJ, Portnoy DA, Calendar R (2002) Construction, characterization, and use of two Listeria monocytogenes sitespecific phage integration vectors. J Bacteriol 184: 4177-4186.
132. Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ (2005) Deconstructing the cadherin-catenin-actin complex. Cell 123: 889-901.
133. Perez TD, Tamada M, Sheetz MP, Nelson WJ (2008) Immediate-early signaling induced by E-cadherin engagement and adhesion. J Biol Chem 283: 5014-5022.
134. Tan S, Tompkins LS, Amieva MR (2009) Helicobacter pylori usurps cell polarity to turn the cell surface into a replicative niche. PLoS Pathog 5: e1000407.
135. Amieva MR, Salama NR, Tompkins LS, Falkow S (2002) Helicobacter pylori enter and survive within multivesicular vacuoles of epithelial cells. Cell Microbiol 4: 677-690.