Entry of human rhinovirus 89 via ICAM-1 into HeLa epithelial cells is inhibited by actin skeleton disruption and by bafilomycin

Archives of Virology

Volumn 159, Issue 1, 2014, Pages 125-140

  Pfanzagl, Beatrix ^a   Andergassen, Daniel ^a   Edlmayr, Johanna ^a   Niespodziana, Katarzyna ^a   Valenta, Rudolf ^a   Blaas, Dieter ^b  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ALEXA; HUMAN RHINOVIRUS 89; HUMAN RHINOVIRUS SP.; RHINOVIRUS;

ACTIN; BAFILOMYCIN A1; CYTOCHALASIN D; INTERCELLULAR ADHESION MOLECULE 1; MACROLIDE; VIRUS RECEPTOR;

ARTICLE; CYTOSKELETON; DRUG EFFECT; ENDOCYTOSIS; EPITHELIUM CELL; GENETICS; HELA CELL; HUMAN; METABOLISM; PHYSIOLOGY; PICORNAVIRUS INFECTION; RHINOVIRUS; VIROLOGY; VIRUS ENTRY;

ACTINS; CYTOCHALASIN D; CYTOSKELETON; ENDOCYTOSIS; EPITHELIAL CELLS; HELA CELLS; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; MACROLIDES; PICORNAVIRIDAE INFECTIONS; RECEPTORS, VIRUS; RHINOVIRUS; VIRUS INTERNALIZATION;

EID: 84893789151     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-013-1797-1     Document Type: Article

References (43)

1. Arden KE, Mackay IM (2010) Newly identified human rhinoviruses: molecular methods heat up the cold viruses. Rev Med Virol 20: 156-176.
2. Bacso Z, Bene L, Damjanovich L, Damjanovich S (2002) INF-gamma rearranges membrane topography of MHC-I and ICAM-1 in colon carcinoma cells. Biochem Biophys Res Commun 290: 635-640.
3. Bourguignon LY, Singleton PA, Diedrich F (2004) Hyaluronan-CD44 interaction with Rac1-dependent protein kinase N-gamma promotes phospholipase Cgamma1 activation, Ca(2+) signaling, and cortactin-cytoskeleton function leading to keratinocyte adhesion and differentiation. J Biol Chem 279: 29654-29669.
4. Brabec-Zaruba M, Pfanzagl B, Blaas D, Fuchs R (2009) Site of human rhinovirus RNA uncoating revealed by fluorescent in situ hybridization. J Virol 83: 3770-3777.
5. Carpen O, Pallai P, Staunton DE, Springer TA (1992) Association of intercellular adhesion molecule-1 (ICAM-1) with actin-containing cytoskeleton and alpha-actinin. J Cell Biol 118: 1223-1234.
6. Chichili GR, Rodgers W (2009) Cytoskeleton-membrane interactions in membrane raft structure. Cell Mol Life Sci 66: 2319-2328.
7. Chung C, Mader CC, Schmitz JC, Atladottir J, Fitchev P, Cornwell ML, Koleske AJ, Crawford SE, Gorelick F (2011) The vacuolar-ATPase modulates matrix metalloproteinase isoforms in human pancreatic cancer. Lab Invest 91: 732-743.
8. Edlmayr J, Niespodziana K, Linhart B, Focke-Tejkl M, Westritschnig K, Scheiblhofer S, Stoecklinger A, Kneidinger M, Valent P, Campana R, Thalhamer J, Popow-Kraupp T, Valenta R (2009) A combination vaccine for allergy and rhinovirus infections based on rhinovirus-derived surface protein VP1 and a nonallergenic peptide of the major timothy grass pollen allergen Phl p 1. J Immunol 182: 6298-6306.
9. Ehrlich M, Boll W, van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118: 591-605.
10. Engel S, Heger T, Mancini R, Herzog F, Kartenbeck J, Hayer A, Helenius A (2011) Role of endosomes in simian virus 40 entry and infection. J Virol 85: 4198-4211.
11. Eyster CA, Higginson JD, Huebner R, Porat-Shliom N, Weigert R, Wu WW, Shen RF, Donaldson JG (2009) Discovery of new cargo proteins that enter cells through clathrin-independent endocytosis. Traffic 10: 590-599.
12. Grunert HP, Wolf KU, Langner KD, Sawitzky D, Habermehl KO, Zeichhardt H (1997) Internalization of human rhinovirus 14 into HeLa and ICAM-1-transfected BHK cells. Med Microbiol Immunol 186: 1-9.
13. Heikkila O, Susi P, Tevaluoto T, Harma H, Marjomaki V, Hyypia T, Kiljunen S (2010) Internalization of coxsackievirus A9 is mediated by {beta}2-microglobulin, dynamin, and Arf6 but not by caveolin-1 or clathrin. J Virol 84: 3666-3681.
14. Hewat EA, Blaas D (1996) Structure of a neutralizing antibody bound bivalently to human rhinovirus 2. EMBO J 15: 1515-1523.
15. Hofer F, Gruenberger M, Kowalski H, Machat H, Huettinger M, Kuechler E, Blaas D (1994) Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc Natl Acad Scie USA 91: 1839-1842.
16. Hoover-Litty H, Greve JM (1993) Formation of rhinovirus-soluble ICAM-1 complexes and conformational changes in the virion. J Virol 67: 390-397.
17. Katoh K, Kano Y, Ookawara S (2007) Rho-kinase dependent organization of stress fibers and focal adhesions in cultured fibroblasts. Genes Cells 12: 623-638.
18. Khan AG, Pickl-Herk A, Gajdzik L, Marlovits TC, Fuchs R, Blaas D (2010) Human rhinovirus 14 enters rhabdomyosarcoma cells expressing icam-1 by a clathrin-, caveolin-, and flotillin-independent pathway. J Virol 84: 3984-3992.
19. Koivusalo M, Welch C, Hayashi H, Scott CC, Kim M, Alexander T, Touret N, Hahn KM, Grinstein S (2010) Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J Cell Biol 188: 547-563.
20. Lawson C, Wolf S (2009) ICAM-1 signaling in endothelial cells. Pharmacol Rep 61: 22-32.
21. Liu G, Place AT, Chen Z, Brovkovych VM, Vogel SM, Muller WA, Skidgel RA, Malik AB, Minshall RD (2012) ICAM-1-activated Src and eNOS signaling increase endothelial cell surface PECAM-1 adhesivity and neutrophil transmigration. Blood 120: 1942-1952.
22. Lonberg-Holm K, Korant BD (1972) Early interaction of rhinoviruses with host cells. J Virol 9: 29-40.
23. Marlovits TC, Abrahamsberg C, Blaas D (1998) Very-low-density lipoprotein receptor fragment shed from HeLa cells inhibits human rhinovirus infection. J Virol 72: 10246-10250.
24. Mercer J, Helenius A (2012) Gulping rather than sipping: macropinocytosis as a way of virus entry. Curr Opin Microbiol 15: 490-499.
25. Mortensen K, Larsson LI (2003) Effects of cytochalasin D on the actin cytoskeleton: association of neoformed actin aggregates with proteins involved in signaling and endocytosis. Cell Mol Life Sci 60: 1007-1012.
26. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63.
27. Muro S, Wiewrodt R, Thomas A, Koniaris L, Albelda SM, Muzykantov VR, Koval M (2003) A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1. J Cell Sci 116: 1599-1609.
28. Muro S, Mateescu M, Gajewski C, Robinson M, Muzykantov VR, Koval M (2006) Control of intracellular trafficking of ICAM-1-targeted nanocarriers by endothelial Na+/H+ exchanger proteins. Am J Physiol Lung Cell Mol Physiol 290: L809-L817.
29. Neubauer C, Frasel L, Kuechler E, Blaas D (1987) Mechanism of entry of human rhinovirus 2 into HeLa cells. Virology 158: 255-258.
30. Newcombe NG, Andersson P, Johansson ES, Au GG, Lindberg AM, Barry RD, Shafren DR (2003) Cellular receptor interactions of C-cluster human group A coxsackieviruses. J Gen Virol 84: 3041-3050.
31. Nurani G, Lindqvist B, Casasnovas JM (2003) Receptor priming of major group human rhinoviruses for uncoating and entry at mild low-pH environments. J Virol 77: 11985-11991.
32. Papademetriou J, Garnacho C, Serrano D, Bhowmick T, Schuchman EH, Muro S (2012) Comparative binding, endocytosis, and biodistribution of antibodies and antibody-coated carriers for targeted delivery of lysosomal enzymes to ICAM-1 versus transferrin receptor. J Inherit Metab Dis 36(3): 467-477.
33. Reed LJ, Muench H (1938) A simple method of estimating fifty percent endpoints. Am J Hyg 27: 493-497.
34. Rejman J, Oberle V, Zuhorn IS, Hoekstra D (2004) Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 377: 159-169.
35. Sennoune SR, Bakunts K, Martinez GM, Chua-Tuan JL, Kebir Y, Attaya MN, Martinez-Zaguilan R (2004) Vacuolar H+-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am J Physiol Cell Physiol 286: C1443-C1452.
36. Snyers L, Zwickl H, Blaas D (2003) Human rhinovirus type 2 is internalized by clathrin-mediated endocytosis. J Virol 77: 5360-5369.
37. Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD, Springer TA (1989) A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56: 849-853.
38. Swanson JA (2008) Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 9: 639-649.
39. Tilghman RW, Hoover RL (2002) E-selectin and ICAM-1 are incorporated into detergent-insoluble membrane domains following clustering in endothelial cells. FEBS Lett 525: 83-87.
40. Tominaga T, Barber DL (1998) Na-H exchange acts downstream of RhoA to regulate integrin-induced cell adhesion and spreading. Mol Biol Cell 9: 2287-2303.
41. Uncapher CR, DeWitt CM, Colonno RJ (1991) The major and minor group receptor families contain all but one human rhinovirus serotype. Virology 180: 814-817.
42. van Dam EM, Ten Broeke T, Jansen K, Spijkers P, Stoorvogel W (2002) Endocytosed transferrin receptors recycle via distinct dynamin and phosphatidylinositol 3-kinase-dependent pathways. J Biol Chem 277: 48876-48883.
43. Zhang S, Liu T, Liang H, Zhang H, Yan D, Wang N, Jiang X, Feng W, Wang J, Li P, Li Z (2009) Lipid rafts uncouple surface expression of transmembrane TNF-alpha from its cytotoxicity associated with ICAM-1 clustering in Raji cells. Mol Immunol 46: 1551-1560.