A lipid zipper triggers bacterial invasion

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

Volumn 111, Issue 35, 2014, Pages 12895-12900

  Eierhoff, Thorsten ^a   Bastian, Björn ^a   Thuenauer, Roland ^a   Madl, Josef ^a   Audfray, Aymeric ^b   Aigal, Sahaja ^a,c   Juillot, Samuel ^a   Rydell, Gustaf E ^d   Mul̈ler, Stefan ^a   De Bentzmann, Sophie ^e   Imberty, Anne ^b   Fleck, Christian ^a,f   Rom̈er, Winfried ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b CENTRE DE RECHERCHES SUR LES MACROMOLÉCULES VÉGÉTALES CERMAV CNRS   (France)

^c International Max Planck Research School for Molecular and Cellular Biology   (Germany)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e CNRS and Aix Marseille University   (France)

^f WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Glycolipid; Infection; Membrane curvature

Indexed keywords

GLYCOLIPID; INFECTION; MEMBRANE CURVATURE;

ACTINS; ADHESINS, BACTERIAL; BACTERIAL ADHESION; CELL MEMBRANE; EPITHELIAL CELLS; GLYCOLIPIDS; GLYCOSPHINGOLIPIDS; LIPID BILAYERS; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SIGNAL TRANSDUCTION; SPHINGOLIPIDS;

EID: 84907228229     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1402637111     Document Type: Article

References (54)

1. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387(6633):569-572.
2. Lingwood CA (2011) Glycosphingolipid functions. Cold Spring Harb Perspect Biol 3(7):a011874.
3. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327(5961):46-50.
4. Riethmüller J, Riehle A, Grassmé H, Gulbins E (2006) Membrane rafts in host-pathogen interactions. Biochim Biophys Acta 1758(12):2139-2147.
5. Lafont F, Abrami L, van der Goot FG (2004) Bacterial subversion of lipid rafts. Curr Opin Microbiol 7(1):4-10.
6. Pizarro-Cerdá J, Cossart P (2006) Bacterial adhesion and entry into host cells. Cell 124(4):715-727.
7. Seveau S, Bierne H, Giroux S, Prévost 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(5):743-753.
8. Chi E, Mehl T, Nunn D, Lory S (1991) Interaction of Pseudomonas aeruginosa with A549 pneumocyte cells. Infect Immun 59(3):822-828.
9. Emam A, Carter WG, Lingwood C (2010) Glycolipid-dependent, protease sensitive internalization of Pseudomonas aeruginosa into cultured human respiratory epithelial cells. Open Microbiol J 4:106-115.
10. Fleiszig SM, Zaidi TS, Fletcher EL, Preston MJ, Pier GB (1994) Pseudomonas aeruginosa invades corneal epithelial cells during experimental infection. Infect Immun 62(8):3485-3493.
11. Ha U, Jin S (2001) Growth phase-dependent invasion of Pseudomonas aeruginosa and its survival within HeLa cells. Infect Immun 69(7):4398-4406.
12. Pereira SH, Cervante MP, Bentzmann S, Plotkowski MC (1997) Pseudomonas aeruginosa entry into Caco-2 cells is enhanced in repairing wounded monolayers. Microb Pathog 23(4):249-255.
13. Plotkowski MC, Meirelles MN (1997) Concomitant endosome-phagosome fusion and lysis of endosomal membranes account for Pseudomonas aeruginosa survival in human endothelial cells. J Submicrosc Cytol Pathol 29(2):229-237.
14. Plotkowski MC, Saliba AM, Pereira SH, Cervante MP, Bajolet-Laudinat O (1994) Pseudomonas aeruginosa selective adherence to and entry into human endothelial cells. Infect Immun 62(12):5456-5463.
15. Fleiszig SM, et al. (1996) Relationship between cytotoxicity and corneal epithelial cell invasion by clinical isolates of Pseudomonas aeruginosa. Infect Immun 64(6):2288-2294.
16. Roger P, et al. (1999) Fibronectin and alpha5beta1 integrin mediate binding of Pseudomonas aeruginosa to repairing airway epithelium. Eur Respir J 13(6):1301-1309.
17. Pier GB, Grout M, Zaidi TS (1997) Cystic fibrosis transmembrane conductance regulator is an epithelial cell receptor for clearance of Pseudomonas aeruginosa from the lung. Proc Natl Acad Sci USA 94(22):12088-12093.
18. Pielage JF, Powell KR, Kalman D, Engel JN (2008) RNAi screen reveals an Abl kinase-dependent host cell pathway involved in Pseudomonas aeruginosa internalization. PLoS Pathog 4(3):e1000031.
19. de Bentzmann S, et al. (1996) Asialo GM1 is a receptor for Pseudomonas aeruginosa adherence to regenerating respiratory epithelial cells. Infect Immun 64(5):1582-1588.
20. Gilboa-Garber N, Sudakevitz D, Sheffi M, Sela R, Levene C (1994) PA-I and PA-II lectin interactions with the ABO(H) and P blood group glycosphingolipid antigens may contribute to the broad spectrum adherence of Pseudomonas aeruginosa to human tissues in secondary infections. Glycoconj J 11(5):414-417.
21. Glick J, Garber N (1983) The intracellular localization of Pseudumonas aeruginosa lectins. J Gen Microbiol 129:3085-3090.
22. Lanne B, Cîopraga J, Bergström J, Motas C, Karlsson KA (1994) Binding of the galactose-specific Pseudomonas aeruginosa lectin, PA-I, to glycosphingolipids and other glycoconjugates. Glycoconj J 11(4):292-298.
23. Gilboa-Garber N (1972) Inhibition of broad spectrum hemagglutinin from Pseudomonas aeruginosa by D-galactose and its derivatives. FEBS Lett 20(2):242-244.
24. Chemani C, et al. (2009) Role of LecA and LecB lectins in Pseudomonas aeruginosa-induced lung injury and effect of carbohydrate ligands. Infect Immun 77(5):2065-2075.
25. Blanchard B, et al. (2008) Structural basis of the preferential binding for globo-series glycosphingolipids displayed by Pseudomonas aeruginosa lectin I. J Mol Biol 383(4):837-853.
26. Cossart P, Sansonetti PJ (2004) Bacterial invasion: The paradigms of enteroinvasive pathogens. Science 304(5668):242-248.
27. Helfrich W (1973) Elastic properties of lipid bilayers: Theory and possible experiments. Z Naturforsch C 28(11):693-703.
28. Reichl L (2009) A Modern Course in Statistical Physics (Wiley-VCH, Weinheim, Germany).
29. Lieber AD, Yehudai-Resheff S, Barnhart EL, Theriot JA, Keren K (2013) Membrane tension in rapidly moving cells is determined by cytoskeletal forces. Curr Biol 23(15):1409-1417.
30. Pietuch A, Brückner BR, Janshoff A (2013) Membrane tension homeostasis of epithelial cells through surface area regulation in response to osmotic stress. Biochim Biophys Acta 1833(3):712-722.
31. Dai J, Sheetz MP (1999) Membrane tether formation from blebbing cells. Biophys J 77(6):3363-3370.
32. Römer W, et al. (2007) Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 450(7170):670-675.
33. Ewers H, et al. (2010) GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 12(1):11-18; sup pp 11-12.
34. Pollard TD, Blanchoin L, Mullins RD (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29:545-576.
35. Coué M, Brenner SL, Spector I, Korn ED (1987) Inhibition of actin polymerization by latrunculin A. FEBS Lett 213(2):316-318.
36. Lingwood D, Ries J, Schwille P, Simons K (2008) Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc Natl Acad Sci USA 105(29):10005-10010.
37. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1(1):31-39.
38. Byfield FJ, Aranda-Espinoza H, Romanenko VG, Rothblat GH, Levitan I (2004) Cholesterol depletion increases membrane stiffness of aortic endothelial cells. Biophys J 87(5):3336-3343.
39. Gracia RS, Bezlyepkina N, Knorr RL, Lipowsky R, Dimova R (2010) Effect of cholesterol on the rigidity of saturated and unsaturated membranes: Fluctuation and electrodeformation analysis of giant vesicles. Soft Matter 6(7):1472-1482.
40. McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V (2009) Salmonella takes control: Effector-driven manipulation of the host. Curr Opin Microbiol 12(1):117-124.
41. Ogawa M, Handa Y, Ashida H, Suzuki M, Sasakawa C (2008) The versatility of Shigella effectors. Nat Rev Microbiol 6(1):11-16.
42. Galán JE, Collmer A (1999) Type III secretion machines: Bacterial devices for protein delivery into host cells. Science 284(5418):1322-1328.
43. Jendrossek V, et al. (2003) Apoptotic response of Chang cells to infection with Pseudomonas aeruginosa strains PAK and PAO-I: Molecular ordering of the apoptosis signaling cascade and role of type IV pili. Infect Immun 71(5):2665-2673.
44. Barbieri JT, Sun J (2004) Pseudomonas aeruginosa ExoS and ExoT. Rev Physiol Biochem Pharmacol 152:79-92.
45. Sana TG, et al. (2012) The second type VI secretion system of Pseudomonas aeruginosa strain PAO1 is regulated by quorum sensing and Fur and modulates internalization in epithelial cells. J Biol Chem 287(32):27095-27105.
46. Römer W, et al. (2010) Actin dynamics drive membrane reorganization and scission in clathrin-independent endocytosis. Cell 140(4):540-553.
47. Peter BJ, et al. (2004) BAR domains as sensors of membrane curvature: The amphiphysin BAR structure. Science 303(5657):495-499.
48. Diggle SP, et al. (2006) The galactophilic lectin, LecA, contributes to biofilm development in Pseudomonas aeruginosa. Environ Microbiol 8(6):1095-1104.
49. Sharon N (2006) Carbohydrates as future anti-adhesion drugs for infectious diseases. Biochim Biophys Acta 1760(4):527-537.
50. 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(5):861-871.
51. Shen Y, Naujokas M, Park M, Ireton K (2000) InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103(3):501-510.
52. Mengaud J, Ohayon H, Gounon P, Cossart P, Cossart P; Mege R-M (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84(6):923-932.
53. Rydell GE, Svensson L, Larson G, Johannes L, Römer W (2013) Human GII.4 norovirus VLP induces membrane invaginations on giant unilamellar vesicles containing secretor gene dependent α1,2-fucosylated glycosphingolipids. Biochim Biophys Acta 1828(8):1840-1845.
54. Mathivet L, Cribier S, Devaux PF (1996) Shape change and physical properties of giant phospholipid vesicles prepared in the presence of an AC electric field. Biophys J 70(3):1112-1121.