Echovirus 1 infection depends on biogenesis of novel multivesicular bodies

Cellular Microbiology

Volumn 13, Issue 12, 2011, Pages 1975-1995

  Karjalainen, Mikko ^a   Rintanen, Nina ^a   Lehkonen, Moona ^a   Kallio, Katri ^b   Mäki, Anita ^a   Hellström, Kirsi ^b   Siljamäki, Valtteri ^a   Upla, Paula ^a   Marjomäki, Varpu ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; VERY LATE ACTIVATION ANTIGEN 2;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; ECHO VIRUS; ECHOVIRUS INFECTION; ENDOSOME; GENE CLUSTER; HUMAN; HUMAN CELL; LYSOSOME; MULTIVESICULAR BODY; NONHUMAN; PH; PRIORITY JOURNAL; VIRUS ENTRY;

CELL LINE, TUMOR; CELL MEMBRANE; CYTOPLASMIC VESICLES; ECHOVIRUS INFECTIONS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENTEROVIRUS B, HUMAN; FLUORESCENCE; HUMANS; HYDROGEN-ION CONCENTRATION; INTEGRIN ALPHA2BETA1; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, VIRUS; RNA, SMALL INTERFERING; TIME FACTORS; TRANSFECTION; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

HUMAN ECHOVIRUS 1; PICORNAVIRIDAE;

EID: 81355146605     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01685.x     Document Type: Article

References (72)

1. Authier, F., Metioui, M., Bell, A.W., and Mort, J.S. (1999) Negative regulation of epidermal growth factor signaling by selective proteolytic mechanisms in the endosome mediated by cathepsin B. J Biol Chem 274: 33723-33731.
2. Azmi, I., Davies, B., Dimaano, C., Payne, J., Eckert, D., Babst, M., and Katzmann, D.J. (2006) Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1. J Cell Biol 172: 705-717.
3. Babst, M., Wendland, B., Estepa, E.J., and Emr, S.D. (1998) The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J 17: 2982-2993.
4. Babst, M., Katzmann, D.J., Estepa-Sabal, E.J., Meerloo, T., and Emr, S.D. (2002) Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell 3: 271-282.
5. Bache, K.G., Brech, A., Mehlum, A., and Stenmark, H. (2003a) Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J Cell Biol 162: 435-442.
6. Bache, K.G., Raiborg, C., Mehlum, A., and Stenmark, H. (2003b) STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J Biol Chem 278: 12513-12521.
7. Bache, K.G., Slagsvold, T., and Stenmark, H. (2004) Defective downregulation of receptor tyrosine kinases in cancer. EMBO J 23: 2707-2712.
8. Bergelson, J.M., Shepley, M.P., Chan, B.M., Hemler, M.E., and Finberg, R.W. (1992) Identification of the integrin VLA-2 as a receptor for echovirus 1. Science 255: 1718-1720.
9. Bishop, P.C., Myers, T., Robey, R., Fry, D.W., Liu, E.T., Blagosklonny, M.V., and Bates, S.E. (2002) Differential sensitivity of cancer cells to inhibitors of the epidermal growth factor receptor family. Oncogene 21: 119-127.
10. Cao, H., Chen, J., Awoniyi, M., Henley, J.R., and McNiven, M.A. (2007) Dynamin 2 mediates fluid-phase micropinocytosis in epithelial cells. J Cell Sci 120: 4167-4177.
11. Caswell, P.T., and Norman, J.C. (2006) Integrin trafficking and the control of cell migration. Traffic 7: 14-21.
12. Cham, B.P., Gerrard, J.M., and Bainton, D.F. (1994) Granulophysin is located in the membrane of azurophilic granules in human neutrophils and mobilizes to the plasma membrane following cell stimulation. Am J Pathol 144: 1369-1380.
13. Chen, X., and Wang, Z. (2001) Regulation of intracellular trafficking of the EGF receptor by Rab5 in the absence of phosphatidylinositol 3-kinase activity. EMBO Rep 2: 68-74.
14. Cieutat, A.M., Lobel, P., August, J.T., Kjeldsen, L., Sengelov, H., Borregaard, N., and Bainton, D.F. (1998) Azurophilic granules of human neutrophilic leukocytes are deficient in lysosome-associated membrane proteins but retain the mannose 6-phosphate recognition marker. Blood 91: 1044-1058.
15. Danielsson, P.E. (1980) Euclidean distance mapping. Comput Graph Image Process 14: 227-248.
16. Engel, S., Heger, T., Mancini, R., Herzog, F., Kartenbeck, J., Hayer, A., and Helenius, A. (2011) Role of endosomes in simian virus 40 entry and infection. J Virol 85: 4198-4211.
17. Fujita, H., Yamanaka, M., Imamura, K., Tanaka, Y., Nara, A., Yoshimori, T., etal. (2003) A dominant negative form of the AAA ATPase SKD1/VPS4 impairs membrane trafficking out of endosomal/lysosomal compartments: class E vps phenotype in mammalian cells. J Cell Sci 116: 401-414.
18. Futter, C.E., Pearse, A., Hewlett, L.J., and Hopkins, C.R. (1996) Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 132: 1011-1023.
19. Garrus, J.E., von Schwedler, U.K., Pornillos, O.W., Morham, S.G., Zavitz, K.H., Wang, H.E., etal. (2001) Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107: 55-65.
20. Gruenberg, J., and Stenmark, H. (2004) The biogenesis of multivesicular endosomes. Nat Rev Mol Cell Biol 5: 317-323.
21. Gruenberg, J., Griffiths, G., and Howell, K.E. (1989) Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J Cell Biol 108: 1301-1316.
22. Hartlieb, B., and Weissenhorn, W. (2006) Filovirus assembly and budding. Virology 344: 64-70.
23. Hayer, A., Stoeber, M., Ritz, D., Engel, S., Meyer, H.H., and Helenius, A. (2010) Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J Cell Biol 191: 615-629.
24. Heijnen, H.F., Schiel, A.E., Fijnheer, R., Geuze, H.J., and Sixma, J.J. (1999) Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 94: 3791-3799.
25. Hirsch, J.G., Fedorko, M.E., and Cohn, Z.A. (1968) Vesicle fusion and formation at the surface of pinocytic vacuoles in macrophages. J Cell Biol 38: 629-632.
26. Ivaska, J., Reunanen, H., Westermarck, J., Koivisto, L., Kahari, V.M., and Heino, J. (1999) Integrin alpha2beta1 mediates isoform-specific activation of p38 and upregulation of collagen gene transcription by a mechanism involving the alpha2 cytoplasmic tail. J Cell Biol 147: 401-416.
27. Jayakar, H.R., Jeetendra, E., and Whitt, M.A. (2004) Rhabdovirus assembly and budding. Virus Res 106: 117-132.
28. Joshi, A., Ablan, S.D., Soheilian, F., Nagashima, K., and Freed, E.O. (2009) Evidence that productive human immunodeficiency virus type 1 assembly can occur in an intracellular compartment. J Virol 83: 5375-5387.
29. Kankaanpaa, P., Paavolainen, L., Marjomaki, V., Heino, J., and White, D.J. (2006) BioImageXD-free open source software for analysis and visualization of multidimensional biomedical images [WWW document].
30. Karjalainen, M., Kakkonen, E., Upla, P., Paloranta, H., Kankaanpaa, P., Liberali, P., etal. (2008) A Raft-derived, Pak1-regulated entry participates in alpha2beta1 integrin-dependent sorting to caveosomes. Mol Biol Cell 19: 2857-2869.
31. Katzmann, D.J., Odorizzi, G., and Emr, S.D. (2002) Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 3: 893-905.
32. Kobayashi, T., Stang, E., Fang, K.S., de Moerloose, P., Parton, R.G., and Gruenberg, J. (1998) A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392: 193-197.
33. Kobayashi, T., Vischer, U.M., Rosnoblet, C., Lebrand, C., Lindsay, M., Parton, R.G., etal. (2000) The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. Mol Biol Cell 11: 1829-1843.
34. Kostelansky, M.S., Schluter, C., Tam, Y.Y., Lee, S., Ghirlando, R., Beach, B., etal. (2007) Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 129: 485-498.
35. Lanz, E., Gregor, M., Slavík, J., and Kotyk, A. (1997) Use of FITC as a fluorescent probe for intracellular pH measurement. J Fluoresc 7: 317-319.
36. Leabu, M., Uniyal, S., Xie, J., Xu, Y.Q., Vladau, C., Morris, V.L., and Chan, B.M. (2005) Integrin alpha2beta1 modulates EGF stimulation of Rho GTPase-dependent morphological changes in adherent human rhabdomyosarcoma RD cells. J Cell Physiol 202: 754-766.
37. Liao, P.-S., Chen, T.-S., and Chung, P.-C. (2001) A fast algorithm for multilevel thresholding. J Inf Sci Eng 17: 713-727.
38. Liberali, P., Kakkonen, E., Turacchio, G., Valente, C., Spaar, A., Perinetti, G., etal. (2008) The closure of Pak1-dependent macropinosomes requires the phosphorylation of CtBP1/BARS. EMBO J 27: 970-981.
39. Liu, Y.W., Surka, M.C., Schroeter, T., Lukiyanchuk, V., and Schmid, S.L. (2008) Isoform and splice-variant specific functions of dynamin-2 revealed by analysis of conditional knock-out cells. Mol Biol Cell 19: 5347-5359.
40. Marjomaki, V., Pietiainen, V., Matilainen, H., Upla, P., Ivaska, J., Nissinen, L., etal. (2002) Internalization of echovirus 1 in caveolae. J Virol 76: 1856-1865.
41. Mercer, J., and Helenius, A. (2009) Virus entry by macropinocytosis. Nat Cell Biol 11: 510-520.
42. Moro, L., Dolce, L., Cabodi, S., Bergatto, E., Boeri Erba, E., Smeriglio, M., etal. (2002) Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines. J Biol Chem 277: 9405-9414.
43. Nickerson, D.P., West, M., Henry, R., and Odorizzi, G. (2010) Regulators of Vps4 ATPase activity at endosomes differentially influence the size and rate of formation of intralumenal vesicles. Mol Biol Cell 21: 1023-1032.
44. van Niel, G., Porto-Carreiro, I., Simoes, S., and Raposo, G. (2006) Exosomes: a common pathway for a specialized function. J Biochem 140: 13-21.
45. Ning, Y., Buranda, T., and Hudson, L.G. (2007) Activated epidermal growth factor receptor induces integrin alpha2 internalization via caveolae/raft-dependent endocytic pathway. J Biol Chem 282: 6380-6387.
46. Otsu, N. (1979) A threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern 9: 62-66.
47. Pawliczek, T., and Crump, C.M. (2009) Herpes simplex virus type 1 production requires a functional ESCRT-III complex but is independent of TSG101 and ALIX expression. J Virol 83: 11254-11264.
48. Pelkmans, L., Kartenbeck, J., and Helenius, A. (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3: 473-483.
49. Pellinen, T., and Ivaska, J. (2006) Integrin traffic. J Cell Sci 119: 3723-3731.
50. Pietiainen, V., Marjomaki, V., Upla, P., Pelkmans, L., Helenius, A., and Hyypia, T. (2004) Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol Biol Cell 15: 4911-4925.
51. Piper, R.C., and Katzmann, D.J. (2007) Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol 23: 519-547.
52. Pons, V., Luyet, P.P., Morel, E., Abrami, L., van der Goot, F.G., Parton, R.G., and Gruenberg, J. (2008) Hrs and SNX3 functions in sorting and membrane invagination within multivesicular bodies. PLoS Biol 6: e214.
53. Raiborg, C., and Stenmark, H. (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458: 445-452.
54. Raiborg, C., Bache, K.G., Gillooly, D.J., Madshus, I.H., Stang, E., and Stenmark, H. (2002) Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol 4: 394-398.
55. Sachse, M., Urbe, S., Oorschot, V., Strous, G.J., and Klumperman, J. (2002) Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol Biol Cell 13: 1313-1328.
56. Sachse, M., Strous, G.J., and Klumperman, J. (2004) ATPase-deficient hVPS4 impairs formation of internal endosomal vesicles and stabilizes bilayered clathrin coats on endosomal vacuoles. J Cell Sci 117: 1699-1708.
57. Sigismund, S., Woelk, T., Puri, C., Maspero, E., Tacchetti, C., Transidico, P., etal. (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci USA 102: 2760-2765.
58. Sigismund, S., Argenzio, E., Tosoni, D., Cavallaro, E., Polo, S., and Di Fiore, P.P. (2008) Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15: 209-219.
59. Slagsvold, T., Aasland, R., Hirano, S., Bache, K.G., Raiborg, C., Trambaiolo, D., etal. (2005) Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J Biol Chem 280: 19600-19606.
60. Slot, J.W., and Geuze, H.J. (2007) Cryosectioning and immunolabeling. Nat Protoc 10: 2480-2491.
61. Soille, P. (2003) Morphological Image Analysis: Principles and Applications. Berlin: Springer.
62. Sorkin, A., and Goh, L.K. (2009) Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 315: 683-696.
63. Takimoto, T., and Portner, A. (2004) Molecular mechanism of paramyxovirus budding. Virus Res 106: 133-145.
64. Tandon, R., AuCoin, D.P., and Mocarski, E.S. (2009) Human cytomegalovirus exploits ESCRT machinery in the process of virion maturation. J Virol 83: 10797-10807.
65. Teis, D., Saksena, S., Judson, B.L., and Emr, S.D. (2010) ESCRT-II coordinates the assembly of ESCRT-III filaments for cargo sorting and multivesicular body vesicle formation. EMBO J 29: 871-883.
66. Theos, A.C., Truschel, S.T., Tenza, D., Hurbain, I., Harper, D.C., Berson, J.F., etal. (2006) A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis. Dev Cell 10: 343-354.
67. Upla, P., Marjomaki, V., Kankaanpaa, P., Ivaska, J., Hyypia, T., Van Der Goot, F.G., and Heino, J. (2004) Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol Biol Cell 15: 625-636.
68. Upla, P., Marjomaki, V., Nissinen, L., Nylund, C., Waris, M., Hyypia, T., and Heino, J. (2008) Calpain 1 and 2 are required for RNA replication of echovirus 1. J Virol 82: 1581-1590.
69. Urata, S., Noda, T., Kawaoka, Y., Yokosawa, H., and Yasuda, J. (2006) Cellular factors required for Lassa virus budding. J Virol 80: 4191-4195.
70. Wollert, T., Wunder, C., Lippincott-Schwartz, J., and Hurley, J.H. (2009) Membrane scission by the ESCRT-III complex. Nature 458: 172-177.
71. Yamanaka, I., Koizumi, M., Baba, T., Yamashita, S., Suzuki, T., and Kudo, R. (2003) Epidermal growth factor increased the expression of alpha2beta1-integrin and modulated integrin-mediated signaling in human cervical adenocarcinoma cells. Exp Cell Res 286: 165-174.
72. Yu, X., Miyamoto, S., and Mekada, E. (2000) Integrin alpha 2 beta 1-dependent EGF receptor activation at cell-cell contact sites. J Cell Sci 113 (Part 12): 2139-2147.