Intrinsic phospholipase A2 activity of adeno-associated virus is involved in endosomal escape of incoming particles

Virology

Volumn 409, Issue 1, 2011, Pages 77-83

  Stahnke, Stefanie ^a   Lux, Kerstin ^b   Uhrig, Silke ^a   Kreppel, Florian ^c   Hösel, Marianna ^a   Coutelle, Oliver ^a   Ogris, Manfred ^b   Hallek, Michael ^a   Büning, Hildegard ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF ULM   (Germany)

Author keywords

AAV serotype 2; Endosomal escape; Lipolytic pore formation; Parvovirus; Phospholipase A2

Indexed keywords

ALANINE; ASPARAGINE; ASPARTIC ACID; HISTIDINE; PHOSPHOLIPASE A2;

ADENO ASSOCIATED VIRUS; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; ENDOSOME; ENDOSOME ESCAPE; ENZYME ACTIVITY; GENETIC COMPLEMENTATION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SEROTYPE; TRANS ISOMER; VIRUS REPLICATION; VIRUS VIRULENCE; WILD TYPE;

CAPSID PROTEINS; DEPENDOVIRUS; ENDOSOMES; HEK293 CELLS; HELA CELLS; HUMANS; MUTATION; PHOSPHOLIPASES A2; SEROTYPING; VIRION;

ADENO-ASSOCIATED VIRUS; MINUTE VIRUS OF MICE; MIRIDAE; PARVOVIRUS;

EID: 78649447518     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.09.025     Document Type: Article

References (30)

1. Balsinde J., Balboa M.A., Insel P.A., Dennis E.A. Regulation and inhibition of phospholipase A2. Annu. Rev. Pharmacol. Toxicol. 1999, 39:175-189.
2. Bleker S., Sonntag F., Kleinschmidt J.A. Mutational analysis of narrow pores at the fivefold symmetry axes of adeno-associated virus type 2 capsids reveals a dual role in genome packaging and activation of phospholipase A2 activity. J. Virol. 2005, 79(4):2528-2540.
3. Buning H., Perabo L., Coutelle O., Quadt-Humme S., Hallek M. Recent developments in adeno-associated virus vector technology. J. Gene Med. 2008, 10(7):717-733.
4. Canaan S., Zadori Z., Ghomashchi F., Bollinger J., Sadilek M., Moreau M.E., Tijssen P., Gelb M.H. Interfacial enzymology of parvovirus phospholipases A2. J. Biol. Chem. 2004, 279(15):14502-14508.
5. Cotmore S.F., Tattersall P. Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 2007, 70:183-232.
6. Dennis E.A. The growing phospholipase A2 superfamily of signal transduction enzymes. Trends Biochem. Sci. 1997, 22(1):1-2.
7. Espenlaub S., Corjon S., Engler T., Fella C., Ogris M., Wagner E., Kochanek S., Kreppel F. Capsomere-specific fluorescent labeling of adenovirus vector particles allows for detailed analysis of intracellular particle trafficking and of the performance of bioresponsive bonds for vector capsid modifications. Hum. Gene Ther. 2010, 21(9):1155-1167.
8. Farr G.A., Zhang L.G., Tattersall P. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc. Natl. Acad. Sci. USA 2005, 102(47):17148-17153.
9. Gastaldelli M., Imelli N., Boucke K., Amstutz B., Meier O., Greber U.F. Infectious adenovirus type 2 transport through early but not late endosomes. Traffic 2008, 9(12):2265-2278.
10. Girod A., Ried M., Wobus C., Lahm H., Leike K., Kleinschmidt J., Deleage G., Hallek M. Genetic capsid modifications allow efficient re-targeting of adeno-associated virus type 2. Nat. Med. 1999, 5(9):1052-1056.
11. 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. 2002, 83(Pt 5):973-978.
12. Grieger J.C., Snowdy S., Samulski R.J. Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J. Virol. 2006, 80(11):5199-5210.
13. Hacker U.T., Wingenfeld L., Kofler D.M., Schuhmann N.K., Lutz S., Herold T., King S.B., Gerner F.M., Perabo L., Rabinowitz J., McCarty D.M., Samulski R.J., Hallek M., Buning H. Adeno-associated virus serotypes 1 to 5 mediated tumor cell directed gene transfer and improvement of transduction efficiency. J. Gene Med. 2005, 7(11):1429-1438.
14. Kramer R.M., Sharp J.D. Structure, function and regulation of Ca2+-sensitive cytosolic phospholipase A2 (cPLA2). FEBS Lett. 1997, 410(1):49-53.
15. Kronenberg S., Bottcher B., von der Lieth C.W., Bleker S., Kleinschmidt J.A. A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini. J. Virol. 2005, 79(9):5296-5303.
16. 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. 2001, 82(Pt 11):2821-2825.
17. Lungwitz U., Breunig M., Blunk T., Gopferich A. Polyethylenimine-based non-viral gene delivery systems. Eur. J. Pharm. Biopharm. 2005, 60(2):247-266.
18. Mudhakir D., Harashima H. Learning from the viral journey: how to enter cells and how to overcome intracellular barriers to reach the nucleus. AAPS J. 2009, 11(1):65-77.
19. Payne C.K., Jones S.A., Chen C., Zhuang X. Internalization and trafficking of cell surface proteoglycans and proteoglycan-binding ligands. Traffic 2007, 8(4):389-401.
20. Sanlioglu S., Benson P.K., Yang J., Atkinson E.M., Reynolds T., Engelhardt J.F. Endocytosis and nuclear trafficking of adeno-associated virus type 2 are controlled by rac1 and phosphatidylinositol-3 kinase activation. J. Virol. 2000, 74(19):9184-9196.
21. Sonntag F., Bleker S., Leuchs B., Fischer R., Kleinschmidt J.A. Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus. J. Virol. 2006, 80(22):11040-11054.
22. Summerford C., Samulski R.J. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 1998, 72(2):1438-1445.
23. Theiss H.D., Kofler D.M., Buning H., Aldenhoff A.L., Kaess B., Decker T., Baumert J., Hallek M., Wendtner C.M. Enhancement of gene transfer with recombinant adeno-associated virus (rAAV) vectors into primary B-cell chronic lymphocytic leukemia cells by CpG-oligodeoxynucleotides. Exp. Hematol. 2003, 31(12):1223-1229.
24. Volpers C., Kochanek S. Adenoviral vectors for gene transfer and therapy. J. Gene Med. 2004, 6(Suppl 1):S164-S171.
25. Warrington K.H., Gorbatyuk O.S., Harrison J.K., Opie S.R., Zolotukhin S., Muzyczka N. Adeno-associated virus type 2 VP2 capsid protein is nonessential and can tolerate large peptide insertions at its N terminus. J. Virol. 2004, 78(12):6595-6609.
26. Wiethoff C.M., Wodrich H., Gerace L., Nemerow G.R. Adenovirus protein VI mediates membrane disruption following capsid disassembly. J. Virol. 2005, 79(4):1992-2000.
27. Xiao X., Li J., Samulski R.J. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol. 1998, 72(3):2224-2232.
28. Xie Q., Somasundaram T., Bhatia S., Bu W., Chapman M.S. Structure determination of adeno-associated virus 2: three complete virus particles per asymmetric unit. Acta Crystallogr. D Biol. Crystallogr. 2003, 59(Pt 6):959-970.
29. Yang S., May S. Release of cationic polymer-DNA complexes from the endosome: a theoretical investigation of the proton sponge hypothesis. J. Chem. Phys. 2008, 129(18):185105.
30. Zadori Z., Szelei J., Lacoste M.C., Li Y., Gariepy S., Raymond P., Allaire M., Nabi I.R., Tijssen P. A viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell 2001, 1(2):291-302.