The adherens junctions control susceptibility to Staphylococcus aureus α-toxin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 46, 2015, Pages 14337-14342

  Popov, Lauren M ^a   Marceau, Caleb D ^a   Starkl, Philipp M ^a   Lumb, Jennifer H ^a   Shah, Jimit ^b   Guerrera, Diego ^b   Cooper, Rachel L ^a   Merakou, Christina ^c   Bouley, Donna M ^a   Meng, Wenxiang ^d,e   Kiyonari, Hiroshi ^f   Takeichi, Masatoshi ^e   Galli, Stephen J ^a   Bagnoli, Fabio ^c   Citi, Sandra ^b   Carette, Jan E ^a   Amieva, Manuel R ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c GSK   (Italy)

^d INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^e RIKEN Center for Biosystems Dynamics Research   (Japan)

^f RIKEN   (Japan)

Author keywords

Adherens junctions; MRSA; PLEKHA7; Staphylococcus aureus; Toxin

Indexed keywords

CYTOPLASM PROTEIN; PLEKSTRIN HOMOLOGY DOMAIN CONTAINING PROTEIN; STAPHYLOCOCCUS ALPHA TOXIN; UNCLASSIFIED DRUG; ADAM PROTEIN; ADAM10 ENDOPEPTIDASE; ADAM10 PROTEIN, HUMAN; ADAM10 PROTEIN, MOUSE; BACTERIAL TOXIN; CARRIER PROTEIN; HEMOLYSIN; MEMBRANE PROTEIN; PLEKHA7 PROTEIN, HUMAN; PLEKHA7 PROTEIN, MOUSE; SECRETASE; STAPHYLOCOCCAL ALPHA-TOXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL JUNCTION; CHANNEL GATING; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; CYTOTOXICITY; GENETIC SCREENING; HAPLOIDY; HUMAN; HUMAN CELL; IN VIVO STUDY; INFECTION SENSITIVITY; INNATE IMMUNITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN INFECTION; SOFT TISSUE INFECTION; STAPHYLOCOCCAL PNEUMONIA; STAPHYLOCOCCUS INFECTION; ADHERENS JUNCTION; ANIMAL; CELL LINE; GENETICS; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; VASCULITIS;

ADAM PROTEINS; ADAM10 PROTEIN; ADHERENS JUNCTIONS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BACTERIAL TOXINS; CARRIER PROTEINS; CELL LINE; HEMOLYSIN PROTEINS; HUMANS; MEMBRANE PROTEINS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; MICE, KNOCKOUT; STAPHYLOCOCCAL INFECTIONS; VASCULITIS;

EID: 84947565955     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1510265112     Document Type: Article

References (53)

1. Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339(8):520-532.
2. Klein E, Smith DL, Laxminarayan R (2007) Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999-2005. Emerg Infect Dis 13(12):1840-1846.
3. Wertheim HFL, et al. (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5(12):751-762.
4. Moran GJ, et al.; EMERGEncy ID Net Study Group (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 355(7):666-674.
5. Klein EY, Sun L, Smith DL, Laxminarayan R (2013) The changing epidemiology of methicillin-resistant Staphylococcus aureus in the United States: A national observational study. Am J Epidemiol 177(7):666-674.
6. De Leo FR, Otto M, Kreiswirth BN, Chambers HF (2010) Community-associated meticillinresistant Staphylococcus aureus. Lancet 375(9725):1557-1568.
7. Bubeck Wardenburg J, Patel RJ, Schneewind O (2007) Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect Immun 75(2):1040-1044.
8. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O (2007) Poring over pores: α-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 13(12):1405-1406.
9. Kennedy AD, et al. (2010) Targeting of alpha-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J Infect Dis 202(7):1050-1058.
10. Kobayashi SD, et al. (2011) Comparative analysis of USA300 virulence determinants in a rabbit model of skin and soft tissue infection. J Infect Dis 204(6):937-941.
11. Song L, et al. (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274(5294):1859-1866.
12. Wilke GA, Bubeck Wardenburg J (2010) Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus α-hemolysin-mediated cellular injury. Proc Natl Acad Sci USA 107(30):13473-13478.
13. Berube BJ, Bubeck Wardenburg J (2013) Staphylococcus aureus a-toxin: Nearly a century of intrigue. Toxins (Basel) 5(6):1140-1166.
14. Haugwitz U, et al. (2006) Pore-forming Staphylococcus aureus alpha-toxin triggers epidermal growth factor receptor-dependent proliferation. Cell Microbiol 8(10):1591-1600.
15. Hruz P, et al. (2009) NOD2 contributes to cutaneous defense against Staphylococcus aureus through alpha-toxin-dependent innate immune activation. Proc Natl Acad Sci USA 106(31):12873-12878.
16. Lizak M, Yarovinsky TO (2012) Phospholipid scramblase 1 mediates type i interferoninduced protection against staphylococcal a-toxin. Cell Host Microbe 11(1):70-80.
17. Maurer K, et al. (2015) Autophagy mediates tolerance to Staphylococcus aureus alpha-toxin. Cell Host Microbe 17(4):429-440.
18. Inoshima I, et al. (2011) A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat Med 17(10):1310-1314.
19. Saftig P, Reiss K (2011) The "A Disintegrin and Metalloproteases" ADAM10 and ADAM17: Novel drug targets with therapeutic potential? Eur J Cell Biol 90(6-7):527-535.
20. Maretzky T, et al. (2005) ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation. Proc Natl Acad Sci USA 102(26):9182-9187.
21. Inoshima N, Wang Y, Bubeck Wardenburg J (2012) Genetic requirement for ADAM10 in severe Staphylococcus aureus skin infection. J Invest Dermatol 132(5):1513-1516.
22. Carette JE, et al. (2009) Haploid genetic screens in human cells identify host factors used by pathogens. Science 326(5957):1231-1235.
23. Carette JE, et al. (2011) Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Nat Biotechnol 29(6):542-546.
24. Meng W, Mushika Y, Ichii T, Takeichi M (2008) Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 135(5):948-959.
25. Haining EJ, et al. (2012) The TspanC8 subgroup of tetraspanins interacts with A disintegrin and metalloprotease 10 (ADAM10) and regulates its maturation and cell surface expression. J Biol Chem 287(47):39753-39765.
26. Gurcel L, Abrami L, Girardin S, Tschopp J, Van Der Goot FG (2006) Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126(6):1135-1145.
27. Im SS, Osborne TF (2012) Protection from bacterial-toxin-induced apoptosis in macrophages requires the lipogenic transcription factor sterol regulatory element binding protein 1a. Mol Cell Biol 32(12):2196-2202.
28. Pulimeno P, Bauer C, Stutz J, Citi S (2010) PLEKHA7 is an adherens junction protein with a tissue distribution and subcellular localization distinct from ZO-1 and E-cadherin. PLoS One 5(8):e12207.
29. Kurita S, Yamada T, Rikitsu E, Ikeda W, Takai Y (2013) Binding between the junctional proteins afadin and PLEKHA7 and implication in the formation of adherens junction in epithelial cells. J Biol Chem 288(41):29356-29368.
30. Citi S, Pulimeno P, Paschoud S (2012) Cingulin, paracingulin, and PLEKHA7: Signaling and cytoskeletal adaptors at the apical junctional complex. Ann N Y Acad Sci 1257:125-132.
31. Paschoud S, Jond L, Guerrera D, Citi S (2014) PLEKHA7 modulates epithelial tight junction barrier function. Tissue Barriers 2(1):e28755.
32. Rodriguez-Boulan E, Nelson WJ (1989) Morphogenesis of the polarized epithelial cell phenotype. Science 245(4919):718-725.
33. Walev I, et al. (1993) Staphylococcal alpha-toxin kills human keratinocytes by permeabilizing the plasma membrane for monovalent ions. Infect Immun 61(12):4972-4979.
34. Husmann M, et al. (2006) Differential role of p38 mitogen activated protein kinase for cellular recovery from attack by pore-forming S. aureus alpha-toxin or streptolysin O. Biochem Biophys Res Commun 344(4):1128-1134.
35. Walev I, et al. (1994) Recovery of human fibroblasts from attack by the pore-forming alpha-toxin of Staphylococcus aureus. Microb Pathog 17(3):187-201.
36. Endres BT, et al. (2014) Mutation of Plekha7 attenuates salt-sensitive hypertension in the rat. Proc Natl Acad Sci USA 111(35):12817-12822.
37. Prabhakara R, et al. (2013) Epicutaneous model of community-acquired Staphylococcus aureus skin infections. Infect Immun 81(4):1306-1315.
38. 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(1):86-93.
39. Sousa S, Lecuit M, Cossart P (2005) Microbial strategies to target, cross or disrupt epithelia. Curr Opin Cell Biol 17(5):489-498.
40. Nikitas G, Cossart P (2012) Adherens junctions and pathogen entry. Subcell Biochem 60:415-425.
41. Kim M, et al. (2010) Bacterial interactions with the host epithelium. Cell Host Microbe 8(1):20-35.
42. Tan S, Tompkins LS, Amieva MR (2009) Helicobacter pylori usurps cell polarity to turn the cell surface into a replicative niche. PLoS Pathog 5(5):e1000407.
43. Tan S, Noto JM, Romero-Gallo J, Peek RM, Jr, Amieva MR (2011) Helicobacter pylori perturbs iron trafficking in the epithelium to grow on the cell surface. PLoS Pathog 7(5):e1002050.
44. Tran CS, et al. (2014) Host cell polarity proteins participate in innate immunity to Pseudomonas aeruginosa infection. Cell Host Microbe 15(5):636-643.
45. Wu S, Morin PJ, Maouyo D, Sears CL (2003) Bacteroides fragilis enterotoxin induces c-Myc expression and cellular proliferation. Gastroenterology 124(2):392-400.
46. Pentecost M, Kumaran J, Ghosh P, Amieva MR (2010) Listeria monocytogenes internalin B activates junctional endocytosis to accelerate intestinal invasion. PLoS Pathog 6(5):e1000900.
47. Zihni C, Balda MS, Matter K (2014) Signalling at tight junctions during epithelial differentiation and microbial pathogenesis. J Cell Sci 127(Pt 16):3401-3413.
48. Larue L, Ohsugi M, Hirchenhain J, Kemler R (1994) E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci USA 91(17):8263-8267.
49. Davis MA, Reynolds AB (2006) Blocked acinar development, E-cadherin reduction, and intraepithelial neoplasia upon ablation of p120-catenin in the mouse salivary gland. Dev Cell 10(1):21-31.
50. Ran FA, et al. (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8(11):2281-2308.
51. Campeau E, et al. (2009) A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS One 4(8):e6529.
52. Bae T, et al. (2004) Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc Natl Acad Sci USA 101(33):12312-12317.
53. Foster TJ (1998) Genetic analysis of staphylococcal virulence. Methods in Microbiology, eds Williams P, Ketley J, Salmond, G (Academic, London), Vol 27, pp 433-454.