Release of canine parvovirus from endocytic vesicles

Virology

Volumn 316, Issue 2, 2003, Pages 267-280

  Suikkanen, Sanna ^a   Antila, Mia ^a   Jaatinen, Anne ^a   Vihinen Ranta, Maija ^a   Vuento, Matti ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

Author keywords

Amiloride; Bafilomycin A1; Brefeldin A; Endocytosis; Entry; Membrane permeabilization; Monensin; Parvovirus; Phospholipase A2; Transferrin receptor

Indexed keywords

AMILORIDE; ANTIBIOTIC AGENT; BAFILOMYCIN A1; BREFELDIN A; DEXTRAN; MONENSIN; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 INHIBITOR; PROTEIN VP1; RHODAMINE; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CAT; CELL PERMEABILIZATION; CONTROLLED STUDY; DOG; ENDOCYTOSIS; ENDOSOME; HEAT; KIDNEY CELL; MOLECULAR WEIGHT; NONHUMAN; PARVOVIRUS; PH; PRIORITY JOURNAL; VIRUS CAPSID; VIRUS INFECTION; VIRUS INFECTIVITY;

CANINE PARVOVIRUS; PARVOVIRUS;

EID: 0344120210     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2003.08.031     Document Type: Article

References (83)

1. Agbandje M., Mckenna R., Rossmann M.G., Strassheim M.L., Parrish C.R. Structure determination of feline panleukopenia virus empty particles. Proteins. 16:(2):1993;155-171.
2. Bartlett J.S., Wilcher R., Samulski R.J. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J. Virol. 74:(6):2000;2777-2785.
3. Basak S., Turner H. Infectious entry pathway for canine parvovirus. Virology. 186:1992;368-376.
4. Bhat S., Spitalnik S.L., Gonzalez-Scarano F., Silberberg D.H. Galactosyl ceramide or a derivative is an essential component of the neural receptor for human immunodeficiency virus type 1 envelope glycoprotein gp120. Proc. Natl. Acad. Sci. USA. 88:(16):1991;7131-7134.
5. Bloom M.E., Alexandersen S., Perryman S., Lechner D., Wolfinbarger J.B. Nucleotide sequence and genomic organization of Aleutian mink disease parvovirus (ADV) sequence comparisons between a nonpathogenic and a pathogenic strain of ADV. J. Virol. 62:(8):1988;2903-2915.
6. Brown K.E., Anderrsson S.M., Young N.S. Erythrocyte P antigen cellular receptor for B19 parvovirus. Science. 262:1993;114-117.
7. Brown W.J., Farquhar M.G. Immunoperoxidase methods for the localization of antigens in cultured cells and tissue sections by electron microscopy. Methods Cell Biol. 31:(553):1989;553-569.
8. Chardonnet Y., Dales S. Early events in the interaction of adenoviruses with HeLa cells. II. Comparative observations on the penetration of types 1, 5, 7, and 12. Virology. 40:(3):1970;478-485.
9. Chen K.C., Shull B.C., Moses E.A., Lederman M., Stout E.R., Bates R.C. Complete nucleotide sequence and genome organization of bovine parvovirus. J. Virol. 60:(3):1986;1085-1097.
10. Clague M.J., Urbé S., Anieto F., Gruenberg J. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem. 269:1994;21-24. (Vacuolar ATPase ECV).
11. Cortes E., San Martin C., Langeveld J., Meloen R., Dalsgaard K., Vela C., Casal I. Topographical analysis of canine parvovirus virions and recombinant VP2 capsids. J. Gen. Virol. 74:(Pt. 9):1993;2005-2010.
12. Cotmore S.E., Tattersall P. The autonomously replicating parvoviruses of vertebrates. Adv. Virus Res. 33:1987;91-169.
13. Cotmore S.F., D'abramo A.M. Jr., Ticknor C.M., Tattersall P. Controlled conformational transitions in the MVM virion expose the VP1 N-terminus and viral genome without particle disassembly. Virology. 254:(1):1999;169-181.
14. Cotmore S.F., D'abramo A.M. Jr., Carbonell L.F., Bratton J., Tattersall P. The NS2 polypeptide of parvorirus MVM is required for capsid assembly in murine cells. Virology. 231:1997;267-280.
15. D'arrigo A., Bucci C., Toh B.H., Stenmark H. Microtubules are involved in bafilomycin A1-induced tubulation and Rab5-dependent vacuolation of early endosomes. Eur. J. Cell. Biol. 72:(2):1997;95-103.
16. Dales S., Chardonnet Y. Early events in the interaction of adenovirus with HeLa cells. Virology. 56:1973;465-483.
17. De Sena J., Mandel B. Studies on the in vitro uncoating of poliovirus. II. Characteristics of the membrane-modified particle. Virology. 78:(2):1977;554-566.
18. Dorsch S., Liebisch G., Kaufmann B., Von Landenberg P., Hoffmann J.H., Drobnik W., Modrow S. The VP1 unique region of parvovirus B19 and its constituent phospholipase A2-like activity. J. Virol. 76:(4):2002;2014-2018.
19. Douar A.M., Poulard K., Stockholm D., Danos O. Intracellular trafficking of adeno-associated virus vectors routing to the late endosomal compartment and proteasome degradation. J. Virol. 75:(4):2001;1824-1833.
20. Fricks C.E., Hogle J.M. Cell-induced conformational change in poliovirus externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64:(5):1990;1934-1945.
21. Gagescu R., Demaurex N., Parton R.G., Hunziker W., Huber L.A., Gruenberg J. The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol. Biol. Cell. 11:(8):2000;2775-2791.
22. Gillooly D.J., Morrow I.C., Lindsay M., Gould R., Bryant N.J., Gaullier J.M., Parton R.G., Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19:(17):2000;4577-4588.
23. Gillooly D.J., Simonsen A., Stenmark H. Cellular functions of phosphatidylinositol 3-phosphate and FYVE domain proteins. Biochem. J. 355:(Pt. 2):2001;249-258.
24. Giranda V.L., Heinz B.A., Oliveira M.A., Minor I., Kim K.H., Kolatkar P.R., Rossmann M.G., Rueckert R.R. Acid-induced structural changes in human rhinovirus 14 possible role in uncoating. Proc. Natl. Acad. Sci. USA. 89:1992;10213-10217.
25. Girod A., Wobus C.E., Zadori Z., Ried M., Leike K., Tijssen P., Kleinschmidt J.A., Hallek M. The VP1 capsid protein of adeno-associated virus type 2 is carrying a phospholipase A2 domain required for virus infectivity. J. Gen. Virol. 83:(Pt. 5):2002;973-978.
26. Gomez Yafal A., Kaplan G., Racaniello V.R., Hogle J.M. Characterization of poliovirus conformational alteration mediated by soluble cell receptors. Virology. 197:(1):1993;501-505.
27. Greve J.M., Forte C.P., Marlor C.W., Meyer A.M., Hoover-Litty H., Wunderlich D., Mcclelland A. Mechanisms of receptor-mediated rhinovirus neutralization defined by two soluble forms of ICAM-1. J. Virol. 65:(11):1991;6015-6023.
28. Gruenberg J. The endocytic pathway a mosaic of domains. Nat. Rev. Mol. Cell. Biol. 2:(10):2001;721-730.
29. Harada M., Shakado S., Sakisaka S., Tamaki S., Ohishi M., Sasatomi K., Koga H., Sata M., Tanikawa K. Bafilomycin A1, a specific inhibitor of V-type H+-ATPases, inhibits the acidification of endocytic structures and inhibits horseradish peroxidase uptake in isolated rat sinusoidal endothelial cells. Liver. 17:(5):1997;244-250.
30. Hendrickson H.S., Hendrickson E.K., Dybvig R.H. Chiral synthesis of a dithiolester analog of phosphatidylcholine as a substrate for the assay of phospholipase A2. J. Lipid Res. 24:(11):1983;1532-1537.
31. Hölttä-Vuori M., Tanhuanpää K., Mobius W., Somerharju P., Ikonen E. Modulation of cellular cholesterol transport and homeostasis by Rab11. Mol. Biol. Cell. 13:(9):2002;3107-3122.
32. Hoover-Litty H., Greve J.M. Formation of rhinovirus-soluble ICAM-1 complexes and conformational changes in the virion. J. Virol. 67:(1):1993;390-397.
33. Johnson L.S., Dunn K.W., Pytowski B., Mcgraw T.E. Endosome acidification and receptor trafficking bafilomycin A1 slows receptor externalization by a mechanism involving the receptor's internalization motif. Mol. Biol. Cell. 4:1993;1251-1266.
34. Jost M., Simpson F., Kavran J.M., Lemmon M.A., Schmid S.L. Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation. Curr. Biol. 8:(25):1998;1399-1402.
35. Juuti-Uusitalo K., Airenne K.J., Laukkanen A., Punnonen E.L., Olkkonen V.M., Gruenberg J., Kulomaa M., Marjomaki V. Selective targeting of avidin/mannose 6-phosphate receptor chimeras to early or late endosomes. Eur. J. Cell. Biol. 79:(7):2000;458-468.
36. Kaplan G., Peters D., Racaniello V.R. Poliovirus mutants resistant to neutralization with soluble cell receptors. Science. 250:(4987):1990;1596-1599.
37. Kim S., Ikeuchi K., Groopman J., Baltimore D. Factors affecting cellular tropism of human immunodeficiency virus. J. Virol. 64:(11):1990;5600-5604.
38. Kobayashi T., Beuchat M.H., Chevallier J., Makino A., Mayran N., Escola J.M., Lebrand C., Cosson P., Gruenberg J. Separation and characterization of late endosomal membrane domains. J. Biol. Chem. 277:(35):2002;32157-32164.
39. Kobayashi T., Stang E., Fang K.S., De Moerloose P., Parton R.G., Gruenberg J. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature. 392:(6672):1998;193-197.
40. Li Y., Zadori Z., Bando H., Dubuc R., Fediere G., Szelei J., Tijssen P. Genome organization of the densovirus from Bombyx mori (BmDNV-1) and enzyme activity of its capsid. J. Gen. Virol. 82:(Pt. 11):2001;2821-2825.
41. Lippincott-Schwartz J., Yuan L., Tipper C., Amherdt M., Orci L., Klausner R.D. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechnism for regulating organelle structure and membrane traffic. Cell. 67:1991;601-616.
42. Marsh E.W., Leopold P.L., Jones N.L., Maxfield F.R. Oligomerized transferrin receptors are selectively retained by a lumenal sorting signal in a long-lived endocytic recycling compartment. J. Cell. Biol. 129:(6):1995;1509- 1522.
43. Marsh M., Helenius A. Virus entry into animal cells. Maramorosch K., Murphy F.A., Shatkin A.J. Advances in Virus Research. Vol. 36:1989;107-151 Academic Press, London.
44. Mayor S., Presley J.F., Maxfield F.R. Sorting of membrane components from endosomes and subsequent recycling to the cell surfase occurs by a bulk flow process. J. Cell Biol. 121:1993;1257-1269.
45. Meier O., Boucke K., Hammer S.V., Keller S., Stidwill R.P., Hemmi S., Greber U.F. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 158:(6):2002;1119-1131.
46. Miyazawa N., Crystal R.G., Leopold P.L. Adenovirus serotype 7 retention in a late endosomal compartment prior to cytosol escape is modulated by fiber protein. J. Virol. 75:(3):2001;1387-1400.
47. Noel J., Pouyssegur J. Hormonal regulation, pharmacology, and membrane sorting of vertebrate Na+/H+ exchanger isoforms. Am. J. Physiol. 268:(2 Pt. 1):1995;C283-C296.
48. Ogier G., Chardonnet Y., Doerfler W. The fate of type 7 adenovirions in lysosomes of HeLa cells. Virology. 77:(1):1977;66-77.
49. Paradiso P.R. Infectious process of the parvovirus H-1 correlation of protein content, particle density, and viral infectivity. J. Virol. 39:(3):1981;800-807.
50. Paradiso P.R., Rhode S.L. 3rd., Singer I.i. Canine parvovirus a biochemical and ultrastructural characterization. J. Gen. Virol. 62:(Pt 1):1982;113-125.
51. Parker J.S., Murphy W.J., Wang D., O'brien S.J., Parrish C.R. Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J. Virol. 75:(8):2001;3896-3902.
52. Parker J.S., Parrish C.R. Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J. Virol. 74:(4):2000;1919-1930.
53. Prchla E., Plank C., Wagner E., Blaas D., Fuchs R. Virus-mediated release of endosomal content in vitro different behavior of adenovirus and rhinovirus serotype 2. J. Cell Biol. 131:(1):1995;111-123.
54. Pressman B.C. Biological applications of ionophores. Annu. Rev. Biochem. 45:1976;501-530.
55. Ros C., Burckhardt C.J., Kempf C. Cytoplasmic trafficking of minute virus of mice low-pH requirement, routing to late endosomes, and proteasome interaction. J. Virol. 76:(24):2002;12634-12645.
56. Ruiz M.C., Alonso-Torre S.R., Charpilienne A., Vasseur M., Michelangeli F., Cohen J., Alvarado F. Rotavirus interaction with isolated membrane vesicles. J. Virol. 68:(6):1994;4009-4016.
57. Seth P., Fitzgerald D.J., Willingham M.C., Pastan I. Role of a low-pH environment in adenovirus enhancement of the toxicity of a Pseudomonas exotoxin-epidermal growth factor conjugate. J. Virol. 51:(3):1984;650-655.
58. Seth P., Willingham M.C., Pastan I. Adenovirus-dependent release of 51Cr from KB cells at an acidic pH. J. Biol. Chem. 259:(23):1984;14350-14353.
59. Seth P., Willingham M.C., Pastan I. Binding of adenovirus and its external proteins to Triton X-114. Dependence on pH. J. Biol. Chem. 260:(27):1985;14431-14434.
60. Shisheva A., Rusin B., Ikonomov O.C., Demarco C., Sbrissa D. Localization and insulin-regulated relocation of phosphoinositide 5-kinase PIKfyve in 3T3-L1 adipocytes. J. Biol. Chem. 276:(15):2001;11859-11869.
61. Simonsen A., Stenmark H. PX domains attracted by phosphoinositides. Nat. Cell. Biol. 3:(8):2001;E179-E182.
62. Simonsen A., Wurmser A.E., Emr S.D., Stenmark H. The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol. 13:(4):2001;485-492.
63. Stein B.S., Sussman H.H. Demonstration of two distinct transferrin receptor recycling pathways and transferrin-independent receptor internalization in K562 cell. J. Biol. Chem. 261:1986;10319-10331.
64. Strassheim M.L., Gruenberg A., Veijalainen P., Sgro J.-Y., Parrish C.R. Two dominant neutralizing antigenic determinants of canine parvovirus are found on the threefold spike of the virus capsid. Virology. 198:1994;175-184.
65. Suikkanen S., Sääjärvi K., Hirsimäki J., Välilehto O., Reunanen H., Vihinen-Ranta M., Vuento M. Role of recycling endosomes and lysosomes in dynein-dependent entry of canine parvovirus. J. Virol. 76:(9):2002;4401-4411.
66. Suomalainen M., Nakano M.Y., Keller S., Boucke K., Stidwill R.P., Greber U.F. Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J. Cell. Biol. 144:(4):1999;657-672.
67. Tattersall P., Cotmore S.F. The nature of parvoviruses. Pattison J.R. Parvoviruses and Human Disease. 1988;5-41 CRC Press, Boca Raton, FL.
68. Tattersall P., Shatkin A.J., Ward D.C. Sequence homology between the structural polypeptides of minute virus of mice. J. Mol. Biol. 111:(4):1977;375-394.
69. Tosteson M.T., Chow M. Characterization of the ion channels formed by poliovirus in planar lipid membranes. J. Virol. 71:(1):1997;507-511.
70. Tsao J., Chapman S., Agbandje M., Keller W., Smith K., Wu H., Luo M., Smith T.J., Rossman M.G., Compans R.W., Parrish C.R. The three-dimensional structure of canine parvovirus and its functional implications. Science. 251:1991;1456-1464.
71. Tullis G.E., Burger L.R., Pintel D.J. The trypsin-sensitive RVER domain in the capsid proteins of minute virus of mice is required for efficient cell binding and viral infection but not for proteolytic processing in vivo. Virology. 191:(2):1992;846-857.
72. Tullis G.E., Burger L.R., Pintel D.J. The minor capsid protein VP1 of autonomous parvovirus minute virus of mice is dispensable for encapsidation of progeny sinle-stranded DNA but is required for infectivity. J. Virol. 67:1993;131-141.
73. Van Weert A.W., Dunn K.W., Gueze H.J., Maxfield F.R., Stoorvogel W. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol. 130:(4):1995;821-834.
74. Vihinen-Ranta M., Kakkola L., Kalela A., Vilja P., Vuento M. Characterization of a nuclear localization signal of canine parvovirus capsid proteins. Eur. J. Biochem. 1:1997;389-394.
75. Vihinen-Ranta M., Kalela A., Mäkinen P., Kakkola L., Marjomäki V., Vuento M. Intracellular route of canine parvovirus entry. J. Virol. 72:1998;802-806.
76. Vihinen-Ranta M., Wang D., Weichert W.S., Parrish C.R. The VP1 N-terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J. Virol. 76:(4):2002;1884-1891.
77. Vihinen-Ranta M., Yuan W., Parrish C.R. Cytoplasmic trafficking of the canine parvovirus capsid and its role in infection and nuclear transport. J. Virol. 74:(10):2000;4853-4859.
78. Weichert W.S., Parker J.S.L., Wahid A.T.M., Chang S.-F., Meier E., Parrish C.R. Assaying for structural variation in the parvovirus capsid and its role in infection. Virology. 250:1998;106-117.
79. Wickham T.J., Filardo E.J., Cheresh D.A., Nemerow G.R. Integrin alpha v beta 5 selectively promotes adenovirus mediated cell membrane permeabilization. J. Cell Biol. 127:(1):1994;257-264.
80. Wikoff W.R., Wang G., Parrish C.R., Cheng R.H., Strassheim M.L., Baker T.S., Rossmann M.G. The structure of a neutralized virus canine parvovirus complexed with neutralizing antibody fragment. Structure. 2:(7):1994;595-607.
81. Xie Q., Chapman M.S. Canine parvovirus capsid structure, analyzed at 2.9 A resolution. J. Mol. Biol. 264:(3):1996;497-520.
82. Yun C.H., Tse C.M., Nath S.K., Levine S.A., Brant S.R., Donowitz M. Mammalian Na+/H+ exchanger gene family structure and function studies. Am. J. Physiol. 269:(1 Pt. 1):1995;G1-G11.
83. 2 is required for parvovirus infectivity. Dev. Cell. 1:2001;291-302.