A capsid-encoded PPxY-motif facilitates adenovirus entry

PLoS Pathogens

Volumn 6, Issue 3, 2010, Pages

  Wodrich, Harald ^a,b,f   Henaff, Daniel ^a,b   Jammart, Baptist ^a,b,g   Segura Morales, Carolina ^a,b,h   Seelmeir, Sigrid ^c   Coux, Olivier ^d   Ruzsics, Zsolt ^c   Wiethoff, Christopher M ^e   Kremer, Eric J ^a,b  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^b UNIV MONTPELLIER   (France)

^c UNIVERSITY OF MUNICH   (Germany)

^d Centre National de la Recherche Scientifique   (France)

^e LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^f University Victor Segalen   (France)

^g INSERM   (France)

^h CENTRE FOR GENOMIC REGULATION CRG   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; PROTEIN VI; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; ESCRT PROTEIN; NEDD4 UBIQUITIN PROTEIN LIGASES; POLYPEPTIDE VI, ADENOVIRUS; UBIQUITIN PROTEIN LIGASE;

ADENOVIRUS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; HUMAN; HUMAN CELL; MICROTUBULE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN TRANSPORT; STRUCTURE ACTIVITY RELATION; UBIQUITINATION; VIRUS CAPSID; VIRUS ENTRY; VIRUS VIRULENCE; CHEMISTRY; CYTOLOGY; ENDOSOME; EPITHELIUM CELL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN ADENOVIRUS; HUMAN ADENOVIRUS INFECTION; LUNG; METABOLISM; MICROTUBULE ORGANIZING CENTER; OSTEOSARCOMA; PHYSIOLOGY; PIGMENT EPITHELIUM; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE; VIROLOGY;

ADENOVIRIDAE; MIRIDAE;

ADENOVIRUS INFECTIONS, HUMAN; ADENOVIRUSES, HUMAN; CAPSID PROTEINS; CELL LINE, TUMOR; CONSERVED SEQUENCE; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; EPITHELIAL CELLS; HUMANS; LUNG; MICROTUBULE-ORGANIZING CENTER; MICROTUBULES; OSTEOSARCOMA; PROTEIN STRUCTURE, TERTIARY; RETINAL PIGMENT EPITHELIUM; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 77950410150     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000808     Document Type: Article

References (57)

1. Brandenburg B, Zhuang X (2007) Virus trafficking - learning from single-virus tracking. Nat Rev Microbiol 5: 197-208. (Pubitemid 46291279)
2. Greber UF, Way M (2006) A superhighway to virus infection. Cell 124: 741-754.
3. Leopold PL, Crystal RG (2007) Intracellular trafficking of adenovirus: many means to many ends. Adv Drug Deliv Rev 59: 810-821.
4. Greber UF (2002) Signalling in viral entry. Cell Mol Life Sci 59: 608-626.
5. Leopold PL, Pfister KK (2006) Viral strategies for intracellular trafficking: motors and microtubules. Traffic 7: 516-523. (Pubitemid 44026750)
6. Bailey CJ, Crystal RG, Leopold PL (2003) Association of adenovirus with the microtubule organizing center. J Virol 77: 13275-13287.
7. Suomalainen M, Nakano MY, Keller S, Boucke K, Stidwill RP, et al. (1999) Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J Cell Biol 144: 657-672. (Pubitemid 29234545)
8. Strunze S, Trotman LC, Boucke K, Greber UF (2005) Nuclear targeting of adenovirus type 2 requires CRM1-mediated nuclear export. Mol Biol Cell 16: 2999-3009. (Pubitemid 40741242)
9. Yu GY, Lai MM (2005) The ubiquitin-proteasome system facilitates the transfer of murine coronavirus from endosome to cytoplasm during virus entry. J Virol 79: 644-648.
10. Khor R, McElroy LJ, Whittaker GR (2003) The ubiquitin-vacuolar protein sorting system is selectively required during entry of influenza virus into host cells. Traffic 4: 857-868. (Pubitemid 37547895)
11. Duan D, Yue Y, Yan Z, Yang J, Engelhardt JF (2000) Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J Clin Invest 105: 1573-1587. (Pubitemid 30390308)
12. Yan Z, Zak R, Luxton GW, Ritchie TC, Bantel-Schaal U, et al. (2002) Ubiquitination of both adeno-associated virus type 2 and 5 capsid proteins affects the transduction efficiency of recombinant vectors. J Virol 76: 2043-2053. (Pubitemid 34150672)
13. Bieniasz PD (2006) Late budding domains and host proteins in enveloped virus release. Virology 344: 55-63.
14. Williams RL, Urbe S (2007) The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol 8: 355-368.
15. Saksena S, Wahlman J, Teis D, Johnson AE, Emr SD (2009) Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136: 97-109.
16. Ingham RJ, Gish G, Pawson T (2004) The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture. Oncogene 23: 1972-1984. (Pubitemid 38496727)
17. Shearwin-Whyatt L, Dalton HE, Foot N, Kumar S (2006) Regulation of functional diversity within the Nedd4 family by accessory and adaptor proteins. Bioessays 28: 617-628. (Pubitemid 43886187)
18. Usami Y, Popov S, Popova E, Gottlinger HG (2008) Efficient and specific rescue of human immunodeficiency virus type 1 budding defects by a Nedd4-like ubiquitin ligase. J Virol 82: 4898-4907.
19. Chung HY, Morita E, von Schwedler U, Muller B, Krausslich HG, et al. (2008) NEDD4L overexpression rescues the release and infectivity of human immunodeficiency virus type 1 constructs lacking PTAP and YPXL late domains. J Virol 82: 4884-4897.
20. Wirblich C, Tan GS, Papaneri A, Godlewski PJ, Orenstein JM, et al. (2008) PPEY motif within the rabies virus (RV) matrix protein is essential for efficient virion release and RV pathogenicity. J Virol 82: 9730-9738.
21. Galinier R, Gout E, Lortat-Jacob H, Wood J, Chroboczek J (2002) Adenovirus protein involved in virus internalization recruits ubiquitin-protein ligases. Biochemistry 41: 14299-14305. (Pubitemid 35403350)
22. Zhang Y, Bergelson JM (2005) Adenovirus receptors. J Virol 79: 12125-12131.
23. Meier O, Greber UF (2004) Adenovirus endocytosis. J Gene Med 6 Suppl 1: S152-163.
24. Rauma T, Tuukkanen J, Bergelson JM, Denning G, Hautala T (1999) rab5 GTPase regulates adenovirus endocytosis. J Virol 73: 9664-9668. (Pubitemid 29487128)
25. Wickham TJ, Mathias P, Cheresh DA, Nemerow GR (1993) Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73: 309-319.
26. Greber UF, Willetts M, Webster P, Helenius A (1993) Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75: 477-486.
27. Greber UF, Webster P, Weber J, Helenius A (1996) The role of the adenovirus protease on virus entry into cells. Embo J 15: 1766-1777. (Pubitemid 26119212)
28. Wiethoff CM, Wodrich H, Gerace L, Nemerow GR (2005) Adenovirus protein VI mediates membrane disruption following capsid disassembly. J Virol 79: 1992-2000. (Pubitemid 40204556)
29. Saphire AC, Guan T, Schirmer EC, Nemerow GR, Gerace L (2000) Nuclear import of adenovirus DNA in vitro involves the nuclear protein import pathway and hsc70. J Biol Chem 275: 4298-4304. (Pubitemid 30094670)
30. Trotman LC, Mosberger N, Fornerod M, Stidwill RP, Greber UF (2001) Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat Cell Biol 3: 1092-1100. (Pubitemid 33130460)
31. Wodrich H, Cassany A, D'Angelo MA, Guan T, Nemerow G, et al. (2006) Adenovirus core protein pVII is translocated into the nucleus by multiple import receptor pathways. J Virol 80: 9608-9618. (Pubitemid 44435635)
32. Loktev AV, Zhang Q, Beck JS, Searby CC, Scheetz TE, et al. (2008) A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev Cell 15: 854-865.
33. Copeland NG, Jenkins NA, Court DL (2001) Recombineering: a powerful new tool for mouse functional genomics. Nat Rev Genet 2: 769-779.
34. Ruzsics Z, Wagner M, Osterlehner A, Cook J, Koszinowski U, et al. (2006) Transposon-assisted cloning and traceless mutagenesis of adenoviruses: Development of a novel vector based on species D. J Virol 80: 8100-8113. (Pubitemid 44182310)
35. Yasuda J, Hunter E (1998) A proline-rich motif (PPPY) in the Gag polyprotein of Mason-Pfizer monkey virus plays a maturation-independent role in virion release. J Virol 72: 4095-4103. (Pubitemid 28188715)
36. Gottwein E, Bodem J, Muller B, Schmechel A, Zentgraf H, et al. (2003) The Mason-Pfizer monkey virus PPPY and PSAP motifs both contribute to virus release. J Virol 77: 9474-9485. (Pubitemid 37011043)
37. Wodrich H, Guan T, Cingolani G, Von Seggern D, Nemerow G, et al. (2003) Switch from capsid protein import to adenovirus assembly by cleavage of nuclear transport signals. Embo J 22: 6245-6255. (Pubitemid 37522582)
38. Martin-Serrano J, Eastman SW, Chung W, Bieniasz PD (2005) HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J Cell Biol 168: 89-101. (Pubitemid 40111060)
39. Gastaldelli M, Imelli N, Boucke K, Amstutz B, Meier O, et al. (2008) Infectious Adenovirus Type 2 Transport Through Early but not Late Endosomes. Traffic.
40. Medina-Kauwe LK (2003) Endocytosis of adenovirus and adenovirus capsid proteins. Adv Drug Deliv Rev 55: 1485-1496.
41. Svensson U (1985) Role of vesicles during adenovirus 2 internalization into HeLa cells. J Virol 55: 442-449.
42. Nakano MY, Boucke K, Suomalainen M, Stidwill RP, Greber UF (2000) The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol. J Virol 74: 7085-7095. (Pubitemid 30470693)
43. Saban SD, Silvestry M, Nemerow GR, Stewart PL (2006) Visualization of alpha-helices in a 6-angstrom resolution cryoelectron microscopy structure of adenovirus allows refinement of capsid protein assignments. J Virol 80: 12049-12059.
44. Russell WC (2009) Adenoviruses: update on structure and function. J Gen Virol 90: 1-20.
45. Fabry CM, Rosa-Calatrava M, Conway JF, Zubieta C, Cusack S, et al. (2005) A quasi-atomic model of human adenovirus type 5 capsid. Embo J 24: 1645-1654. (Pubitemid 40704975)
46. Neumann G, Ebihara H, Takada A, Noda T, Kobasa D, et al. (2005) Ebola virus VP40 late domains are not essential for viral replication in cell culture. J Virol 79: 10300-10307. (Pubitemid 41098571)
47. Morita E, Sandrin V, Chung HY, Morham SG, Gygi SP, et al. (2007) Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. Embo J 26: 4215-4227. (Pubitemid 47525161)
48. Fejer G, Drechsel L, Liese J, Schleicher U, Ruzsics Z, et al. (2008) Key role of splenic myeloid DCs in the IFN-alphabeta response to adenoviruses in vivo. PLoS Pathog 4: e1000208. doi:10.1371/journal.ppat.1000208.
49. Chroboczek J, Gout E, Favier AL, Galinier R (2003) Novel partner proteins of adenovirus penton. Curr Top Microbiol Immunol 272: 37-55. (Pubitemid 36458324)
50. Salinas S, Bilsland LG, Henaff D, Weston AE, Keriel A, et al. (2009) CAR-associated vesicular transport of an adenovirus in motor neuron axons. PLoS Pathog 5: e1000442.
51. Mittereder N, March KL, Trapnell BC (1996) Evaluation of the concentration and bioactivity of adenovirus vectors for gene therapy. J Virol 70: 7498-7509. (Pubitemid 26339054)
52. Segura-Morales C, Pescia C, Chatellard-Causse C, Sadoul R, Bertrand E, et al. (2005) Tsg101 and Alix interact with murine leukemia virus Gag and cooperate with Nedd4 ubiquitin ligases during budding. J Biol Chem 280: 27004-27012. (Pubitemid 41040737)
53. Fotia AB, Ekberg J, Adams DJ, Cook DI, Poronnik P, et al. (2004) Regulation of neuronal voltage-gated sodium channels by the ubiquitin-protein ligases Nedd4 and Nedd4-2. J Biol Chem 279: 28930-28935. (Pubitemid 38915761)
54. Rossi M, Aqeilan RI, Neale M, Candi E, Salomoni P, et al. (2006) The E3 ubiquitin ligase Itch controls the protein stability of p63. Proc Natl Acad Sci U S A 103: 12753-12758. (Pubitemid 44298633)
55. Bubeck A, Wagner M, Ruzsics Z, Lotzerich M, Iglesias M, et al. (2004) Comprehensive mutational analysis of a herpesvirus gene in the viral genome context reveals a region essential for virus replication. J Virol 78(15): 8026-8035. (Pubitemid 38944287)
56. Cherepanov PP, Wackernagel W (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158(1): 9-14.
57. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG (2005) Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33(4): e36.