Integrin-Mediated Signaling Induced by Simian Virus 40 Leads to Transient Uncoupling of Cortical Actin and the Plasma Membrane

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Stergiou, Lilli ^a,d   Bauer, Manuel ^a   Mair, Waltraud ^a   Bausch Fluck, Damaris ^a   Drayman, Nir ^c   Wollscheid, Bernd ^a   Oppenheim, Ariella ^c   Pelkmans, Lucas ^a,b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d Redbiotec AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CLATHRIN; EZRIN; GRAF1 PROTEIN; INTEGRIN; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOGAP PROTEIN; SPHINGOLIPID; SPHINGOLIPID GM1; UNCLASSIFIED DRUG;

ARTICLE; BRAIN CORTEX; CELL ADHESION; CELL COMPONENT; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENDOCYTOSIS; ENZYME ACTIVATION; EPISTASIS; EPITHELIUM CELL; HUMAN; HUMAN CELL; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PROTEIN ANALYSIS; PROTEIN BINDING; RNA INTERFERENCE; SCORING SYSTEM; SIGNAL TRANSDUCTION; SIMIAN VIRUS 40; SIMIAN VIRUS INFECTION; VIRUS INFECTION;

ACTINS; ANIMALS; CELL ADHESION; CELL LINE; CELL MEMBRANE; CYTOSKELETAL PROTEINS; EPISTASIS, GENETIC; GENE REGULATORY NETWORKS; GLYCOSPHINGOLIPIDS; HUMANS; INTEGRINS; MEMBRANE GLYCOPROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; POLYOMAVIRUS INFECTIONS; PROTEIN BINDING; PROTEIN INTERACTION MAPS; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SIMIAN VIRUS 40; VIRUS INTERNALIZATION;

EID: 84873578370     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055799     Document Type: Article

References (50)

1. Anderson HA, Chen Y, Norkin LC, (1996) Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol Biol Cell 7(11): 1825-1834.
2. Chen Y, Norkin LC, (1999) Extracellular simian virus 40 transmits a signal that promotes virus enclosure within caveolae. Exp Cell Res 246(1): 83-90.
3. Pelkmans L, Kartenbeck J, Helenius A, (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3(5): 473-483.
4. Tsai B, Gilbert JM, Stehle T, Lencer W, Benjamin TL, et al. (2003) Gangliosides are receptors for murine polyoma virus and SV40. EMBO J 22(17): 4346-4355.
5. Pelkmans L, Püntener D, Helenius A, (2002) Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296(5567): 535-539.
6. Mundy DI, Machleidt T, Ying Y-s, Anderson RGW, Bloom GS, (2002) Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J Cell Sci 115: 4327-4339.
7. Pelkmans L, Zerial M, (2005) Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436(7047): 128-133.
8. Ewers H, Römer W, Smith AE, Bacia K, Dmitrieff S, et al. (2010) GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 12(1): 11-18.
9. Pelkmans L, Fava E, Grabner H, Hannus M, Habermann B, et al. (2005) Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436(7047): 78-86.
10. Wollscheid B, Bausch-Fluck D, Henderson C, O'Brien R, Bibel M, et al. (2009) Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat Biotechnol 27(4): 378-86.
11. Hofmann A, Gerrits B, Schmidt A, Bock T, Bausch-Fluck D, et al. (2010) Proteomic cell surface phenotyping of differentiating acute myeloid leukemia cells. Blood 116(13): e26-34.
12. Lundmark R, Doherty GJ, Howes MT, Cortese K, Vallis Y, et al. (2008) The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr Biol 18(22): 1802-1808.
13. Hansen CG, Nichols BJ, (2009) Molecular mechanisms of clathrin-independent endocytosis. J Cell Sci 122(Pt 11): 1713-1721.
14. Scherf U, Ross DT, Waltham M, Smith LH, Lee JK, et al. (2000) A gene expression database for the molecular pharmacology of cancer. Nat Genet 24(3): 236-244.
15. Tsukita S, Yonemura S, (1999) Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J Biol Chem 274(49): 34507-34510.
16. Niggli V, Rossy J, (2008) Ezrin/radixin/moesin: versatile controllers of signaling molecules and of the cortical cytoskeleton. Int J Biochem Cell Biol 40(3): 344-349.
17. Weinreb PH, Simon KJ, Rayhorn P, Yang WJ, Leone DR, et al. (2004) Function-blocking integrin alphavbeta6 monoclonal antibodies: distinct ligand-mimetic and nonligand-mimetic classes. J Biol Chem 279(17): 17875-17887.
18. Chu JJ, Ng ML, (2004) Interaction of West Nile virus with alpha v beta 3 integrin mediates virus entry into cells. J Biol Chem 279(52): 54533-54541.
19. Siebers MC, Walboomers XF, van den Dolder J, Leeuwenburgh SC, Wolke JG, et al. (2008) The behavior of osteoblast-like cells on various substrates with functional blocking of integrin-beta1 and integrin-beta3. J Mater Sci Mater Med 19(2): 861-868.
20. Sharma DK, Brown JC, Cheng Z, Holicky EL, Marks DL, et al. (2005) The glycosphingolipid, lactosylceramide, regulates beta1-integrin clustering and endocytosis. Cancer Res 65(18): 8233-8241.
21. Palazzo AF, Eng CH, Schlaepfer DD, Marcantonio EE, Gundersen GG, (2004) Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 303(5659): 836-839.
22. Smith AE, Lilie H, Helenius A, (2003) Ganglioside-dependent cell attachment and endocytosis of murine polyomavirus-like particles. FEBS Lett 555(2): 199-203.
23. Ichikawa S, Nakajo N, Sakiyama H, Hirabayashi Y, (1994) A mouse B16 melanoma mutant deficient in glycolipids. Proc Natl Acad Sci USA 91: 2703-2707.
24. Sandalon Z, Oppenheim A, (1997) Self-assembly and protein-protein interactions between the SV40 capsid proteins produced in insect cells. Virology 237(2): 414-21.
25. Butin-Israeli V, Drayman N, Oppenheim A, (2010) Simian virus 40 infection triggers a balanced network that includes apoptotic, survival, and stress pathways. J Virol 84(7): 3431-3442.
26. Stokoe D, Stephens LR, Copeland T, Gaffney PR, Reese CB, et al. (1997) Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science. 277(5325): 567-570.
27. Lasserre R, Guo XJ, Conchonaud F, Hamon Y, Hawchar O, et al. (2008) Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat Chem Biol 4(9): 538-547.
28. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L, Coppolino MG, Radeva G, et al. (1996) Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 379(6560): 91-96.
29. Wu C, Dedhar S, (2001) Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J Cell Biol 155(4): 505-510.
30. Legate KR, Montañez E, Kudlacek O, Fässler R, (2006) ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 7(1): 20-31.
31. Persad S, Attwell S, Gray V, Mawji N, Deng JT, et al. (2001) Regulation of protein kinase B/Akt-serine 473 phosphorylation by integrin-linked kinase: critical roles for kinase activity and amino acids arginine 211 and serine 343. J Biol Chem 276(29): 27462-27469.
32. Shaw RJ, Henry M, Solomon F, Jacks T, (1998) RhoA-dependent phosphorylation and relocalization of ERM proteins into apical membrane/actin protrusions in fibroblasts. Mol Biol Cell. 9(2): 403-419.
33. Stewart PL, Nemerow GR, (2007) Cell integrins: commonly used receptors for diverse viral pathogens. Trends Microbiol 15(11): 500-507.
34. Zoppi N, Gardella R, De Paepe A, Barlati S, Colombi M, (2004) Human fibroblasts with mutations in COL5A1 and COL3A1 genes do not organize collagens and fibronectin in the extracellular matrix, down-regulate alpha2beta1 integrin, and recruit alphavbeta3 Instead of alpha5beta1 integrin. J Biol Chem 279(18): 18157-68.
35. Pelkmans L, (2005) Secrets of caveolae- and lipid raft-mediated endocytosis revealed by mammalian viruses. Biochim Biophys Acta 1746(3): 295-304.
36. Cheng ZJ, Singh RD, Marks DL, Pagano RE, (2006) Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids. Mol Membr Biol 23(1): 101-110.
37. Matsui T, Maeda M, Doi Y, Yonemura S, Amano M, et al. (1998) Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J Cell Biol 140(3): 647-657.
38. Simons PC, Pietromonaco SF, Reczek D, Bretscher A, Elias L, (1998) C-terminal threonine phosphorylation activates ERM proteins to link the cell's cortical lipid bilayer to the cytoskeleton. Biochem Biophys Res Commun 253(3): 561-565.
39. Ng T, Parsons M, Hughes WE, Monypenny J, Zicha D, et al. (2001) Ezrin is a downstream effector of trafficking PKC-integrin complexes involved in the control of cell motility. EMBO J 20(11): 2723-2741.
40. Charras GT, Hu CK, Coughlin M, Mitchison TJ, (2006) Reassembly of contractile actin cortex in cell blebs. J Cell Biol 175(3): 477-490.
41. Tagawa A, Mezzacasa A, Hayer A, Longatti A, Pelkmans L, et al. (2005) Assembly and trafficking of caveolar domains in the cell: caveolae as stable, cargo-triggered, vesicular transporters. J Cell Biol 170(5): 769-79.
42. Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, et al. (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168(3): 477-488.
43. Sinha B, Köster D, Ruez R, Gonnord P, Bastiani M, et al. (2011) Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 144(3): 402-413.
44. Shibata H, Oishi K, Yamagiwa A, Matsumoto M, Mukai H, et al. (2001) PKNbeta interacts with the SH3 domains of Graf and a novel Graf related protein, Graf2, which are GTPase activating proteins for Rho family. J Biochem 130(1): 23-31.
45. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39(Database issue): D561-8.
46. Barsky A, Gardy JL, Hancock RE, Munzner T, (2007) Cerebral: a Cytoscape plugin for layout of and interaction with biological networks using subcellular localization annotation. Bioinformatics 23(8): 1040-2.
47. Rämö P, Sacher R, Snijder B, Begemann B, Pelkmans L, (2009) CellClassifier: supervised learning of cellular phenotypes. Bioinformatics 25(22): 3028-3030.
48. Deutsch EW, Mendoza L, Shteynberg D, Farrah T, Lam H, et al. (2010) A guided tour of the Trans-Proteomic Pipeline. Proteomics 10(6): 1150-1159.
49. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, et al. (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7(10): R100.
50. Stauffer TP, Ahn S, Meyer T, (1998) Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr Biol 8: 343-346.