Rotavirus infectious particles use lipid rafts during replication for transport to the cell surface in vitro and in vivo

Virology

Volumn 313, Issue 1, 2003, Pages 308-321

  Cuadras, Mariela A ^a,b   Greenberg, Harry B ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; LIPID; VIRUS PROTEIN;

ARTICLE; CELL CYCLE; CELL SURFACE; CONFOCAL MICROSCOPY; DENSITY GRADIENT; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; ROTAVIRUS; VIRUS INFECTION; VIRUS REPLICATION;

MURINAE; MURINE ROTAVIRUS; RHESUS ROTAVIRUS; ROTAVIRUS;

EID: 0041386550     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0042-6822(03)00326-X     Document Type: Article

References (53)

1. Anderson R.G. Caveolae where incoming and outgoing messengers meet . Proc. Natl. Acad. Sci. USA. 90:(23):1993;10909-109013.
2. Bagnat M., Keranen S., Shevchenko A., Simons K. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. USA. 97:(7):2000;3254-3259.
3. Ball, J.M., Parr, R.D., Zhou, M., Storey, S., Schroeder, F., 2002. Role of caveolin-1 in the intracellular transport of rotavirus NSP4, in: 21st Annual Meeting of the American Society for Virology, Virology, A.S.f. (Ed.). University of Kentucky, Lexington, KY.
4. Ball J.M., Tian P., Zeng C.Q., Morris A.P., Estes M.K. Age-dependent diarrhea induced by a rotaviral nonstructural glycoprotein. Science. 272:(5258):1996;101-104.
5. Bresee J.S., Glass R.I., Ivanoff B., Gentsch J.R. Current status and future priorities for rotavirus vaccine development, evaluation and implementation in developing countries. Vaccine. 17:(18):1999;2207-2222.
6. Broome R.L., Vo P.T., Ward R.L., Clark H.F., Greenberg H.B. Murine rotavirus genes encoding outer capsid proteins VP4 and VP7 are not major determinants of host range restriction and virulence. J. Virol. 67:(5):1993;2448-2455.
7. Brown D.A., London E. Structure and origin of ordered lipid domains in biological membranes. J. Membr. Biol. 164:(2):1998;103-114.
8. Brown D.A., Rose J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:(3):1992;533-544.
9. Campbell S.M., Crowe S.M., Mak J. Lipid rafts and HIV-1 from viral entry to assembly of progeny virions . J. Clin. Virol. 22:(3):2001;217-227.
10. Casey P.J. Protein lipidation in cell signaling. Science. 268:(5208):1995;221-225.
11. Clayson E.T., Brando L.V., Compans R.W. Release of simian virus 40 virions from epithelial cells is polarized and occurs without cell lysis. J. Virol. 63:(5):1989;2278-2288.
12. Cuadras M.A., Feigelstock D.A., An S., Greenberg H.B. Gene expression pattern in Caco-2 cells following rotavirus infection. J. Virol. 76:(9):2002;4467-4482.
13. Dormitzer P.R., Ho D.Y., Mackow E.R., Mocarski E.S., Greenberg H.B. Neutralizing epitopes on herpes simplex virus-1-expressed rotavirus VP7 are dependent on coexpression of other rotavirus proteins. Virology. 187:(1):1992;18-32.
14. Estes, M.K. 2001. Rotaviruses and Their Replication in Fields Virology. fourth ed., 2. 2 vols. Lippincott Williams & Wilkins, Philadelphia.
15. Falconer M.M., Gilbert J.M., Roper A.M., Greenberg H.B., Gavora J.S. Rotavirus-induced fusion from without in tissue culture cells. J. Virol. 69:(9):1995;5582-5591.
16. Fenton R.G., Kung H.F., Longo D.L., Smith M.R. Regulation of intracellular actin polymerization by prenylated cellular proteins. J. Cell. Biol. 117:(2):1992;347-356.
17. Franco M.A., Tin C., Greenberg H.B. CD8+ T cells can mediate almost complete short-term and partial long-term immunity to rotavirus in mice. J. Virol. 71:(5):1997;4165-4170.
18. Gonzalez R.A., Espinosa R., Romero P., Lopez S., Arias C.F. Relative localization of viroplasmic and endoplasmic reticulum-resident rotavirus proteins in infected cells. Arch. Virol. 145:(9):2000;1963-1973.
19. Harder T., Scheiffele P., Verkade P., Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell. Biol. 141:(4):1998;929-942.
20. Hauri H.P., Kappeler F., Andersson H., Appenzeller C. ERGIC-53 and traffic in the secretory pathway. J. Cell. Sci. 113:(Pt. 4):2000;587-596.
21. Heino S., Lusa S., Somerharju P., Ehnholm C., Olkkonen V.M., Ikonen E. Dissecting the role of the golgi complex and lipid rafts in biosynthetic transport of cholesterol to the cell surface. Proc. Natl. Acad. Sci. USA. 97:(15):2000;8375-8380.
22. Huang H., Schroeder F., Zeng C., Estes M.K., Schoer J.K., Ball J.M. Membrane interactions of a novel viral enterotoxin rotavirus nonstructural glycoprotein NSP4 . Biochemistry. 40:(13):2001;4169-4180.
23. Jourdan N., Maurice M., Delautier D., Quero A.M., Servin A.L., Trugnan G. Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J. Virol. 71:(11):1997;8268-8278.
24. Kabcenell A.K., Atkinson P.H. Processing of the rough endoplasmic reticulum membrane glycoproteins of rotavirus SA11. J. Cell. Biol. 101:(4):1985;1270-1280.
25. Keller P., Simons K. Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell. Biol. 140:(6):1998;1357-1367.
26. Kilsdonk E.P., Yancey P.G., Stoudt G.W., Bangerter F.W., Johnson W.J., Phillips M.C., Rothblat G.H. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 270:(29):1995;17250-17256.
27. Kundu A., Avalos R.T., Sanderson C.M., Nayak D.P. Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCK cells. J. Virol. 70:(9):1996;6508-6515.
28. Lindwasser O.W., Resh M.D. Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J. Virol. 75:(17):2001;7913-7924.
29. Lizano M., Lopez S., Arias C.F. The amino-terminal half of rotavirus SA114fM VP4 protein contains a hemagglutination domain and primes for neutralizing antibodies to the virus. J. Virol. 65:(3):1991;1383-1391.
30. Maass D.R., Atkinson P.H. Rotavirus proteins VP7, NS28, and VP4 form oligomeric structures. J. Virol. 64:(6):1990;2632-2641.
31. Manes S., del Real G., Lacalle R.A., Lucas P., Gomez-Mouton C., Sanchez-Palomino S., Delgado R., Alcami J., Mira E., Martinez A.C. Membrane raft microdomains mediate lateral assemblies required for HIV-1 infection. EMBO Rep. 1:(2):2000;190-196.
32. Mirazimi A., von Bonsdorff C.H., Svensson L. Effect of brefeldin A on rotavirus assembly and oligosaccharide processing. Virology. 217:(2):1996;554-563.
33. Orlandi P.A., Fishman P.H. Filipin-dependent inhibition of cholera toxin evidence for toxin internalization and activation through caveolae-like domains . J. Cell. Biol. 141:(4):1998;905-915.
34. Parton R.G., Lindsay M. Exploitation of major histocompatibility complex class I molecules and caveolae by simian virus 40. Immunol. Rev. 168:1999;23-31.
35. Pickl W.F., Pimentel-Muinos F.X., Seed B. Lipid rafts and pseudotyping. J. Virol. 75:(15):2001;7175-7183.
36. Resh M.D. Myristylation and palmitylation of Src family members the fats of the matter . Cell. 76:(3):1994;411-413.
37. Ruiz M.C., Abad M.J., Charpilienne A., Cohen J., Michelangeli F. Cell lines susceptible to infection are permeabilized by cleaved and solubilized outer layer proteins of rotavirus. J. Gen. Virol. 78:(Pt 11):1997;2883-2893.
38. Sapin C., Colard O., Delmas O., Tessier C., Breton M., Enouf V., Chwetzoff S., Ouanich J., Cohen J., Wolf C., Trugnan G. Rafts promote assembly and atypical targeting of a nonenveloped virus, rotavirus, in Caco-2 cells. J. Virol. 76:(9):2002;4591-4602.
39. Sargiacomo M., Sudol M., Tang Z., Lisanti M.P. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell. Biol. 122:(4):1993;789-807.
40. Scheiffele P., Rietveld A., Wilk T., Simons K. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 274:(4):1999;2038-2044.
41. Scheiffele P., Roth M.G., Simons K. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16:(18):1997;5501-5508.
42. Sevlever D., Pickett S., Mann K.J., Sambamurti K., Medof M.E., Rosenberry T.L. Glycosylphosphatidylinositol-anchor intermediates associate with triton-insoluble membranes in subcellular compartments that include the endoplasmic reticulum. Biochem. J. 343:(Pt 3):1999;627-635.
43. Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 387:(6633):1997;569-572.
44. Simons K., Ikonen E. How cells handle cholesterol. Science. 290:(5497):2000;1721-1726.
45. Simons K., van Meer G. Lipid sorting in epithelial cells. Biochemistry. 27:(17):1988;6197-6202.
46. Simons K., Wandinger-Ness A. Polarized sorting in epithelia. Cell. 62:(2):1990;207-210.
47. Skibbens J.E., Roth M.G., Matlin K.S. Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and nonpolar fibroblasts. J. Cell. Biol. 108:(3):1989;821-832.
48. Stahl A., Hirsch D.J., Gimeno R.E., Punreddy S., Ge P., Watson N., Patel S., Kotler M., Raimondi A., Tartaglia L.A., Lodish H.F. Identification of the major intestinal fatty acid transport protein. Mol. Cell. 4:(3):1999;299-308.
49. Tucker S.P., Thornton C.L., Wimmer E., Compans R.W. Vectorial release of poliovirus from polarized human intestinal epithelial cells. J. Virol. 67:(7):1993;4274-4282.
50. Vincent S., Gerlier D., Manie S.N. Measles virus assembly within membrane rafts. J. Virol. 74:(21):2000;9911-9915.
51. Werling D., Hope J.C., Chaplin P., Collins R.A., Taylor G., Howard C.J. Involvement of caveolae in the uptake of respiratory syncytial virus antigen by dendritic cells. J. Leukoc. Biol. 66:(1):1999;50-58.
52. Xu A., Bellamy A.R., Taylor J.A. Immobilization of the early secretory pathway by a virus glycoprotein that binds to microtubules. EMBO J. 19:(23):2000;6465-6474.
53. Zhang M., Zeng C.Q., Morris A.P., Estes M.K. A functional NSP4 enterotoxin peptide secreted from rotavirus-infected cells. J. Virol. 74:(24):2000;11663-11670.