Rotavirus assembly: An alternative model that utilizes an atypical trafficking pathway

Current Topics in Microbiology and Immunology

Volumn 309, Issue , 2006, Pages 245-261

  Chwetzoff, S ^a   Trugnan, G ^a  

^a HÔPITAL SAINT ANTOINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHOLESTEROL; FLOTILLIN 1; FLOTILLIN 2; HEAT SHOCK PROTEIN 70; PROTEIN VP4; RAB PROTEIN; SPHINGOLIPID; TUNICAMYCIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; CAPSID PROTEIN; VP4 PROTEIN, ROTAVIRUS;

APICAL MEMBRANE; CELL MEMBRANE; CYTOLYSIS; CYTOSKELETON; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HYPOTHESIS; INTESTINE CELL; INTESTINE EPITHELIUM CELL; INTESTINE INFECTION; KIDNEY CELL; KIDNEY EPITHELIUM; LIPID RAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; ROTAVIRUS; VIRUS ASSEMBLY; VIRUS MORPHOLOGY; ANIMAL; BIOLOGICAL MODEL; INTESTINE MUCOSA; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; VIROLOGY;

ROTAVIRUS;

ANIMALS; CAPSID PROTEINS; ENTEROCYTES; HUMANS; INTESTINAL MUCOSA; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; ROTAVIRUS; VIRAL PROTEINS; VIRUS ASSEMBLY;

EID: 33748114368     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/3-540-30773-7_9     Document Type: Review

References (79)

1. Aït Slimane T, Lenoir C, Sapin C, Maurice M, Trugnan G (2000) Apical secretion and sialylation of soluble dipeptidyl-peptidase-IV are two related events. Exp Cell Res 257:184-194
2. Aït Slimane T, Lenoir C, Bello V, Delaunay J-L, Goding JW, Chwetzoff S, Maurice M, Fransen JAM, Trugnan G (2001) The cytoplasmic/transmembrane domain of DPPIV, a type II glycoprotein, contains an apical targeting signal that does not specifically interact with lipid rafts. Exp Cell Res 270:45-55
3. Au KS, Mattion NM, Estes MK (1993) A subviral particle binding domain on the rotavirus nonstructural glycoprotein NS28. Virology 194:665-673
4. Blutt SE, Kirkwood CD, Parreno V, Warfield KL, Ciarlet M, Estes MK, Bok K, Bishop RF, Conner ME (2003) Rotavirus antigenaemia and viraemia: a common event? Lancet 362:1445-1449
5. Braccia A, Villani M, Immerdal, L, Niels-Christiansen LL, Nystrom BT, Hansen GH, Danielsen EM (2003) Microvillar membrane microdomains exist at physiological temperature. Role of galectin-4 as lipid raft stabilizer revealed by superrafts. J Biol Chem 278:15679-15684
6. Bremont M, Juste-Lesage P, Chabanne-Vautherot D, Charpilienne A, Cohen J (1992) Sequences of the four larger proteins of a porcine group C rotavirus and comparison with the equivalent group A rotavirus proteins. Virology 186:684-692. Erratum in: Virology (1992) 189:402
7. Broquet AH, Thomas G, Masliah J, Trugnan G, Bachelet M (2003) Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J Biol Chem 278:21601-21606
8. Brunet JP, Cotte-Laffitte J, Linxe C, Quero AM, Geniteau-Legendre M, Servin A (2000a) Rotavirus infection induces an increase in intracellular calcium concentration in human intestinal epithelial cells: role in microvillar actin alteration. J Virol 74:2323-2332
9. Brunet JP, Jourdan N, Cotte-Laffitte J, Linxe C, Geniteau-Legendre M, Servin A, Quero AM (2000b) Rotavirus infection induces cytoskeleton disorganization in human intestinal epithelial cells: implication of an increase in intracellular calcium concentration. J Virol 74:10801-10806
10. Chantret I, Barbat A, Dussaulx E, Brattain MG, Zweibaum A (1988) Epithelial polarity, villin expression, and enterocytic differentiation of cultured human colon carcinoma cells: a survey of twenty cell lines. Cancer Res 48:1936-1942
11. Chazal N, Gerlier D (2003) Virus entry, assembly, budding, and membrane rafts. Microbiol Mol Biol Rev 67:226-237
12. Ciarlet M, Crawford SE, Estes MK (2001) Differential infection of polarized epithelial cell lines by sialic acid-dependent and sialic acid-independent rotavirus strains. J Virol 75:11834-11850
13. Couet J, Li S, Okamoto T, Ikezu T, Lisanti MP (1997) Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 272:6525-6533
14. Cuadras MA, Greenberg HB (2003) Rotavirus infectious particles use lipid rafts during replication for transport to the cell surface in vitro and in vivo. Virology 313:308-321
15. Danielsen EM, Hansen GH (2003) Lipid rafts in epithelial brush borders: atypical membrane microdomains with specialized functions. Biochim Biophys Acta 1617:1-9
16. Danielsen EM, van Deurs B, Hansen GH, (2003). Nonclassical secretion of annexin A2 to the lumenal side of the enterocyte brush border membrane. Biochemistry 42:14670-14676
17. Darmoul D, Lacasa M, Baricault L, Marguet D, Sapin C, Trotot P, Trugnan G (1992) Dipeptidylpeptidase IV (DPP IV,CD26) gene expression in enterocyte-like colon cancer cell lines HT-29 and Caco-2. Cloning of the complete human coding sequence and changes of DPP IV mRNA levels during cell differentiation. J Biol Chem 267:4824-4833
18. Dector MA, Romero P, Lopez S, Arias CF (2002) Rotavirus gene silencing by small interfering RNAs. EMBO Rep 3:1175-1180
19. Delmas O, Durand-Schneider AM, Cohen J, Colard O, Trugnan G (2004a) Spike protein VP4 assembly with maturing rotavirus requires a postendoplasmic reticulum event in polarized caco-2 cells. J Virol 78:10987-10994
20. Delmas O, Gardet A, Chwetzoff S, Breton M, Cohen J, Colard O, Sapin C, Trugnan G (2004b) Different ways to reach the top of a cell. Analysis of rotavirus assembly and targeting in human intestinal cells reveals an original raft-dependent, Golgi-independent apical targeting pathway. Virology 327:157-161
21. Delorme C, Brüssow H, Sidoti J, Roche N, Karlsson KA, Neeser JR, Teneberg S (2001) Glycosphingolipid binding specificities of rotavirus: identification of a sialic acid-binding epitope. J Virol 75:2276-2287
22. Dormitzer PR, Sun ZY, Wagner G, Harrison SC (2002) The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 21:885-897
23. Dormitzer PR, Nason EB, Prasad BV, Harrison SC (2004) Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430:1053-1058
24. Enouf V, Chwetzoff S, Trugnan G, Cohen J (2003) Interactions of rotavirus VP4 spike protein with the endosomal protein Rab5 and the prenylated Rab acceptor PRA1. J Virol 77:7041-7047
25. th edn. Lippincott Williams and Wilkins, Philadelphia, pp 1747-1785
26. Faure AV, Migne C, Devilliers G, Ayala-Sanmartin J (2002) Annexin 2 "secretion" accompanying exocytosis of chromaffin cells: possible mechanisms of annexin release. Exp. Cell Res 276:79-89
27. Golantsova NE, Gorbunova EE, Mackow ER (2004) Discrete domains within the rotavirus VP5 direct peripheral membrane association and membrane permeability. J Virol 78:2037-2044
28. Gonzalez RA, Espinosa R, Romero P, Lopez S, Arias CF (2000) Relative localization of viroplasmic and endoplasmic reticulum-resident rotavirus proteins in infected cells. Arch Virol 145:1963-1973
29. Hanada K, Kumagai K, Yasuda S, Miura Y, Kawano M, Fukasawa M, Nishijima M (2003) Molecular machinery for non-vesicular trafficking of ceramide. Nature 426:803-809
30. Hansen GH, Immerdal L, Thorsen E, Niels-Christiansen LL, Nystrom BT, Demant EJ, Danielsen EM (2001) Lipid rafts exist as stable cholesterol- independent microdomains in the brush border membrane of enterocytes. J Biol Chem276:32338-32344
31. Helms JB, Zurzolo C (2004) Lipids as targeting signals: lipid rafts and intracellular trafficking Traffic 5:247-254
32. Hoekstra D, van Ijzendoorn SCD (2000) Lipid trafficking and sorting: how cholesterol is filling gaps. Curr Opin Cell Biol 12:496-502
33. Holthuis JC, Pomorski T, Raggers RJ, Sprong H, Van Meer G (2001) The organizing potential of sphingolipids in intracellular membrane transport. Physiol Rev 81:1689-1723
34. Huang H, Schroeder F, Zeng C, Estes MK, Schoer JK, Ball JM (2001) Membrane interactions of a novel viral enterotoxin: rotavirus nonstructural glycoprotein NSP4. Biochemistry 40:4169-4180
35. Isa P, Realpe M, Romero P, Lopez S, Arias CF (2004) Rotavirus RRV associates with lipid membrane microdomains during cell entry. Virology 322:370-381. Erratum in: Virology (2004) 328:158
36. Jayaram H, Estes MK, Prasad BV (2004) Emerging themes in rotavirus cell entry, genome organization, transcription and replication. Virus Res 101:67-81
37. Jourdan N, Maurice M, Delautier D, Quero AM, Servin AL, Trugnan G (1997) Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J Virol 71:8268-8278
38. Jourdan N, Brunet JP, Sapin C, Blais A, Cotte-Laffitte J, Forestier F, Quero AM, Trugnan G, Servin AL (1998) Rotavirus infection reduces sucrase-isomaltase expression in human intestinal epithelial cells by perturbing protein targeting and organization of microvillar cytoskeleton. J Virol 72:7228-7236
39. Kabcenell AK, Poruchynsky MS, Bellamy AR, Greenberg HB, Atkinson PH (1988) Two forms of VP7 are involved in assembly of SA11 rotavirus in endoplasmic reticulum. J Virol 62:2929-2941
40. Lawton JA, Estes MK, Prasad BV (2000) Mechanism of genome transcription in segmented dsRNA viruses. Adv Virus Res 55:185-229
41. Lipardi C, Nitsch L, Zurzolo C (2000) Detergent-insoluble GPI-anchored proteins are apically sorted in Fischer rat thyroid cells, but interference with cholesterol or sphingolipids differentially affects detergent insolubility and apical sorting. Mol Biol Cell 11:531-542
42. Lopez S, Arias CF (2004) Multistep entry of rotavirus into cells: a Versaillesque dance. Trends Microbiol 12:271-278
43. Maass DR, Atkinson PH (1990) Rotavirus proteins VP7, NS28, and VP4 form oligomeric structures. J Virol 64:2632-2641
44. Mathieu M, Petitpas I, Navaza J, Lepault J, Kohli E, Pothier P, Prasad BV, Cohen J, Rey FA (2001) Atomic structure of the major capsid protein of rotavirus: implications for the architecture of the virion. EMBO J 20:1485-1497
45. Mayor S, Riezman H (2004) Sorting GPI anchored proteins. Nat Rev Mol Cell Biol 5:110-120
46. Mirazimi A, Svensson L (1998) Carbohydrates facilitate correct disulfide bond formation and folding of rotavirus VP7. J Virol 72:3887-3892
47. Mirazimi A, von Bonsdorff CH, Svensson L (1996) Effect of brefeldin A on rotavirus assembly and oligosaccharide processing. Virology 217:554-563
48. Mirre C, Monlauzeur L, Garcia M, Delgrossi MH, Le Bivic A (1996) Detergent-resistant membrane microdomains from Caco-2 cells do not contain caveolin. Am J Physiol 271:C887-C889
49. Mohan KV, Som I, Atreya CD (2002) Identification of a type 1 peroxisomal targeting signal in a viral protein and demonstration of its targeting to the organelle. J Virol 76:2543-2547
50. Mostov KE, Verges M, Altschuler Y (2000) Membrane traffic in polarized epithelial cells. Curr Opin Cell Biol 12:483-490
51. Mostov K, Su T, ter Beest M (2003) Polarized epithelial membrane traffic: conservation and plasticity. Nat Cell Biol 5:287-293
52. Munro S (2003) Lipid rafts: elusive or illusive? Cell 115:377-388
53. Nava P, Lopez S, Arias CF, Islas S, Gonzalez-Mariscal L (2004) The rotavirus surface protein VP8 modulates the gate and fence function of tight junctions in epithelial cells. J Cell Sci 117:5509-5519
54. Nejmeddine M, Trugnan G, Sapin C, Kohli E, Svensson L, Lopez S, Cohen J (2000) Rotavirus spike protein VP4 is present at the plasma membrane and is associated with microtubules in infected cells. J Virol 74:3313-3320
55. Nickel W, (2003) The mystery of non classical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem 270:2109-2119
56. Nguyen DG, Booth A, Gould SJ, Hildreth JE (2003) Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J Biol Chem 278:52347-52354
57. Obert G, Peiffer I, Servin AL (2000) Rotavirus-induced structural and functional alterations in tight junctions of polarized intestinal Caco-2 cell monolayers. J Virol 74:4645-4651
58. Parashar UD, Hummelman EG, Bresee JS, Miller MA, Glass RI (2003) Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 9:565-572
59. Petrie BL, Graham DY, Hanssen H, Estes MK (1982) Localization of rotavirus antigens in infected cells by ultrastructural immunocytochemistry. J Gen Virol 63:457-467
60. Petrie BL, Estes MK, Graham DY (1983) Effects of tunicamycin on rotavirus morphogenesis and infectivity. J Virol 46:270-274
61. Polishchuk R, Di Pentima A, Lippincott-Schwartz J (2004) Delivery of raft-associated, GPI-anchored proteins to the apical surface of polarized MDCK cells by a transcytotic pathway. Nat Cell Biol 6:297-307
62. Prentice E, Jerome WG, Yoshimori T, Mizushima N, Denison MR (2004) Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 279:10136-10141
63. Rajho Meerson N, Bello V, Delaunay J-L, Aït Slimane T, Delautier D, Lenoir C, Trugnan G, Maurice M (2000) Intracellular traffic of the ecto-nucleotide pyrophosphatase/phosphodiesterase NPP3 to the apical plasma membrane of MDCK and Caco-2 cells: apical targeting occurs in the absence of N-glycosylation. J Cell Sci 113:4193-4202
64. Ruiz MC, Cohen J, Michelangeli F (2000) Role of Ca 2+ in the replication and pathogenesis of rotavirus and other viral infections. Cell Calcium 28:137-149
65. Sanchez-San Martin C, Lopez T, Arias CF, Lopez S (2004) Characterization of rotavirus cell entry. J Virol 78:2310-2318
66. Sapin C, Colard O, Delmas O, Tessier C, Breton M, Enouf V, Chwetzoff S, Ouanich J, Cohen J, Wolf C, Trugnan G (2002) Rafts promote assembly and atypical targeting of a nonenveloped virus, rotavirus, in Caco-2 cells. J Virol 76:4591-4602
67. Sarnataro D, Campana V, Paladino S, Stornaiuolo M, Nitsch L, Zurzolo C (2004) PrP(C) association with lipid rafts in the early secretory pathway stabilizes its cellular conformation. Mol Biol Cell 15:4031-4042
68. Schuck S, Honsho M, Ekroos K, Shevchenko A, Simons K (2003) Resistance of cell membranes to different detergents. Proc Natl Acad Sci U S A 100:5795-5800
69. Simons K, Ikonnen E (1997) Functional rafts in cell membranes. Nature 387:569-572
70. Simons K, Vaz WLC (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33:269-295
71. Singer SJ, Nicolson GL (1972) The fluid mosaic model of cell membranes. Science 175:720-731
72. Stirzaker SC, Poncet D, Both GW (1990) Sequences in rotavirus glycoprotein VP7 that mediate delayed translocation and retention of the protein in the endoplasmic reticulum. J Cell Biol 111:1343-1350
73. Struck DK, Lennarz WJ (1977) Evidence for the participation of saccharide-lipids in the synthesis of the oligosaccharide chain of ovalbumin. J Biol Chem 252:1007-1013
74. Suzuki H, Konno T, Numazaki Y (1993) Electron microscopic evidence for budding process-independent assembly of double-shelled rotavirus particles during passage through endoplasmic reticulum membranes. J Gen Virol 74:2015-2018
75. Svensson L, Finlay BB, Bass D, von Bonsdorff CH, Greenberg HB (1991) Symmetric infection of rotavirus on polarized human intestinal epithelial (Caco-2) cells. J Virol 65:4190-4197
76. Taylor JA, O'Brien JA, Lord VJ, Meyer JC, Bellamy AR (1993) The RER-localized intracellular rotavirus receptor: a truncated soluble form is multivalent and bind rotavirus particles. Virology 194:807-814
77. Trugnan G, Rousset M, Chantret I, Barbat A, Zweibaum A (1987) The posttranslational processing of sucrase-isomaltase in HT-29 cells is a function of their state of enterocytic differentiation. J Cell Biol 104:1199-1205
78. Xu A, Bellamy AR, Taylor JA (2000) Immobilization of the early secretory pathway by a virus glycoprotein that binds to microtubules. EMBO J 19:6465-6474
79. Zarate S, Cuadras MA, Espinosa R, Romero P, Juarez KO, Camacho-Nuez M, Arias CF, Lopez S (2003) Interaction of rotaviruses with Hsc70 during cell entry is mediated by VP5. J Virol 77:7254-7260