The host phosphoinositide 5-phosphatase SHIP2 regulates dissemination of vaccinia virus

Journal of Virology

Volumn 85, Issue 14, 2011, Pages 7402-7410

  McNulty, Shannon ^a,c   Powell, Kimberly ^a   Erneux, Christophe ^b   Kalman, Daniel ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PHOSPHATASE; PHOSPHOTYROSINE; PROTEIN A34; PROTEIN SHIP2; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; NONHUMAN; POXVIRUS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; VACCINIA VIRUS; VIRION; VIRUS CELL INTERACTION; VIRUS MUTATION; VIRUS RELEASE; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; CELL LINE; COMET ASSAY; HUMANS; MICE; PHOSPHORIC MONOESTER HYDROLASES; RNA INTERFERENCE; VACCINIA VIRUS;

POXVIRIDAE; VACCINIA VIRUS;

EID: 79960401712     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02391-10     Document Type: Article

References (82)

1. Blasco, R., and B. Moss. 1991. Extracellular vaccinia virus formation and cell-to-cell virus transmission are prevented by deletion of the gene encoding the 37,000-dalton outer envelope protein. J. Virol. 65:5910-5920.
2. Blasco, R., and B. Moss. 1992. Role of cell-associated enveloped vaccinia virus in cell-to-cell spread. J. Virol. 66:4170-4179.
3. Blasco, R., J. R. Sisler, and B. Moss. 1993. Dissociation of progeny vaccinia virus from the cell membrane is regulated by a viral envelope glycoprotein: effect of a point mutation in the lectin homology domain of the A34R gene. J. Virol. 67:3319-3325.
4. Bommarius, B., et al. 2007. Enteropathogenic Escherichia coli Tir is an SH2/3 ligand that recruits and activates tyrosine kinases required for pedestal formation. Mol. Microbiol. 63:1748-1768.
5. Chi, Y., et al. 2004. Comparative mechanistic and substrate specificity study of inositol polyphosphate 5-phosphatase Schizosaccharomyces pombe synaptojanin and SHIP2. J. Biol. Chem. 279:44987-44995.
6. Clement, S., et al. 2001. The lipid phosphatase SHIP2 controls insulin sensitivity. Nature 409:92-97.
7. Damen, J. E., et al. 1996. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc. Natl. Acad. Sci. U. S. A. 93:1689-1693.
8. Dodding, M. P., and M. Way. 2009. Nckand N-WASP-dependent actinbased motility is conserved in divergent vertebrate poxviruses. Cell Host Microbe 6:536-550.
9. Douglas, J. L., et al. 2010. The great escape: viral strategies to counter BST-2/tetherin. PLoS Pathog. 6:e1000913.
10. Duncan, S. A., and G. L. Smith. 1992. Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress. J. Virol. 66:1610-1621.
11. Dyson, J. M., et al. 2001. The SH2-containing inositol polyphosphate 5-phosphatase, SHIP-2, binds filamin and regulates submembraneous actin. J. Cell Biol. 155:1065-1079.
12. Fenner, F. 1996. Poxviruses, p. 2673-2702. In D. M. Knipe et al. (ed.), Fields virology, 3rd ed. Lippincott Williams & Wilkins, Philadelphia, PA.
13. Frischknecht, F., et al. 1999. Tyrosine phosphorylation is required for actinbased motility of vaccinia but not Listeria or Shigella. Curr. Biol. 9:89-92.
14. Frischknecht, F., et al. 1999. Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401:926-929.
15. Geada, M. M., I. Galindo, M. M. Lorenzo, B. Perdiguero, and R. Blasco. 2001. Movements of vaccinia virus intracellular enveloped virions with GFP tagged to the F13L envelope protein. J. Gen. Virol. 82:2747-2760.
16. Giuriato, S., et al. 2002. SHIP2 overexpression strongly reduces the proliferation rate of K562 erythroleukemia cell line. Biochem. Biophys. Res. Commun. 296:106-110.
17. Gouin, E., M. D. Welch, and P. Cossart. 2005. Actin-based motility of intracellular pathogens. Curr. Opin. Microbiol. 8:35-45.
18. Habib, T., J. A. Hejna, R. E. Moses, and S. J. Decker. 1998. Growth factors and insulin stimulate tyrosine phosphorylation of the 51C/SHIP2 protein. J. Biol. Chem. 273:18605-18609.
19. Herrera, E., M. M. Lorenzo, R. Blasco, and S. N. Isaacs. 1998. Functional analysis of vaccinia virus B5R protein: essential role in virus envelopment is independent of a large portion of the extracellular domain. J. Virol. 72:294-302.
20. Hollinshead, M., et al. 2001. Vaccinia virus utilizes microtubules for movement to the cell surface. J. Cell Biol. 154:389-402.
21. Hollinshead, M., A. Vanderplasschen, G. L. Smith, and D. J. Vaux. 1999. Vaccinia virus intracellular mature virions contain only one lipid membrane. J. Virol. 73:1503-1517.
22. Honeychurch, K. M., G. Yang, R. Jordan, and D. E. Hruby. 2007. The vaccinia virus F13L YPPL motif is required for efficient release of extracellular enveloped virus. J. Virol. 81:7310-7315.
23. Ishida, S., et al. 2006. Association of SH-2 containing inositol 5'-phosphatase 2 gene polymorphisms and hyperglycemia. Pancreas 33:63-67.
24. Kagawa, S., et al. 2005. Impact of SRC homology 2-containing inositol 5'-phosphatase 2 gene polymorphisms detected in a Japanese population on insulin signaling. J. Clin. Endocrinol. Metab. 90:2911-2919.
25. Kaisaki, P. J., et al. 2004. Polymorphisms in type II SH2 domain-containing inositol 5-phosphatase (INPPL1, SHIP2) are associated with physiological abnormalities of the metabolic syndrome. Diabetes 53:1900-1904.
26. Kalman, D., et al. 1999. Enteropathogenic E. coli acts through WASP and Arp2/3 complex to form actin pedestals. Nat. Cell Biol. 1:389-391.
27. Kavanaugh, W. M., et al. 1996. Multiple forms of an inositol polyphosphate 5-phosphatase form signaling complexes with Shc and Grb2. Curr. Biol. 6:438-445.
28. Khodakevich, L., Z. Jezek, and D. Messinger. 1988. Monkeypox virus: ecology and public health significance. Bull. World Health Organ. 66:747-752.
29. Khodakevich, L., M. Szczeniowski, D. Manbu ma, Z. Jezek, S. Marennikova, J. Nakano, and D. Messinger. 1987. The role of squirrels in sustaining monkeypox virus transmission. Trop. Geogr. Med. 39:115-122.
30. Krause, M., et al. 2004. Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7:571-583.
31. Lioubin, M. N., et al. 1996. p150Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev. 10:1084-1095.
32. Liu, Y., and V. A. Bankaitis. 2010. Phosphoinositide phosphatases in cell biology and disease. Prog. Lipid Res. 49:201-217.
33. Marion, E., et al. 2002. The gene INPPL1, encoding the lipid phosphatase SHIP2, is a candidate for type 2 diabetes in rat and man. Diabetes 51:2012-2017.
34. McIntosh, A. A., and G. L. Smith. 1996. Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus. J. Virol. 70:272-281.
35. McNulty, S., et al. 2010. Multiple phosphatidylinositol 3-kinases regulate vaccinia virus morphogenesis. PLoS One 5:e10884.
36. Meiser, A., D. Boulanger, G. Sutter, and J. Krijnse Locker. 2003. Comparison of virus production in chicken embryo fibroblasts infected with the WR, IHD-J, and MVA strains of vaccinia virus: IHD-J is most efficient in trans- Golgi network wrapping and extracellular enveloped virus release. J. Gen. Virol. 84:1383-1392.
37. Moreau, V., et al. 2000. A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nat. Cell Biol. 2:441-448.
38. Nakatsu, F., et al. 2010. The inositol 5-phosphatase SHIP2 regulates endocytic clathrin-coated pit dynamics. J. Cell Biol. 190:307-315.
39. Newsome, T. P., N. Scaplehorn, and M. Way. 2004. SRC mediates a switch from microtubuleto actin-based motility of vaccinia virus. Science 306:124-129.
40. Newsome, T. P., I. Weisswange, F. Frischknecht, and M. Way. 2006. Abl collaborates with Src family kinases to stimulate actin-based motility of vaccinia virus. Cell Microbiol. 8:233-241.
41. Onnockx, S., et al. 2008. The association between the SH2-containing inositol polyphosphate 5-phosphatase 2 (SHIP2) and the adaptor protein APS has an impact on biochemical properties of both partners. J. Cell. Physiol. 214:260-272.
42. Parrish, S., and B. Moss. 2006. Characterization of a vaccinia virus mutant with a deletion of the D10R gene encoding a putative negative regulator of gene expression. J. Virol. 80:553-561.
43. Paternotte, N., et al. 2005. SHIP2 interaction with the cytoskeletal protein vinexin. FEBS J. 272:6052-6066.
44. Payne, L. G. 1979. Identification of the vaccinia hemagglutinin polypeptide from a cell system yielding large amounts of extracellular enveloped virus. J. Virol. 31:147-155.
45. Perdiguero, B., and R. Blasco. 2006. Interaction between vaccinia virus extracellular virus envelope A33 and B5 glycoproteins. J. Virol. 80:8763-8777.
46. Perdiguero, B., M. M. Lorenzo, and R. Blasco. 2008. Vaccinia virus A34 glycoprotein determines the protein composition of the extracellular virus envelope. J. Virol. 82:2150-2160.
47. Pesesse, X., S. Deleu, F. De Smedt, L. Drayer, and C. Erneux. 1997. Identification of a second SH2-domain-containing protein closely related to the phosphatidylinositol polyphosphate 5-phosphatase SHIP. Biochem. Biophys. Res. Commun. 239:697-700.
48. Pesesse, X., et al. 2001. The Src homology 2 domain containing inositol 5-phosphatase SHIP2 is recruited to the epidermal growth factor (EGF) receptor and dephosphorylates phosphatidylinositol 3,4,5-trisphosphate in EGF-stimulated COS-7 cells. J. Biol. Chem. 276:28348-28355.
49. Pesesse, X., et al. 1998. The SH2 domain containing inositol 5-phosphatase SHIP2 displays phosphatidylinositol 3,4,5-trisphosphate and inositol 1,3,4,5tetrakisphosphate 5-phosphatase activity. FEBS Lett. 437:301-303.
50. Prasad, N., R. S. Topping, and S. J. Decker. 2001. SH2-containing inositol 5'-phosphatase SHIP2 associates with the p130Cas adapter protein and regulates cellular adhesion and spreading. Mol. Cell. Biol. 21:1416-1428.
51. Prasad, N. K., and S. J. Decker. 2005. SH2-containing 5'-inositol phosphatase, SHIP2, regulates cytoskeleton organization and ligand-dependent down-regulation of the epidermal growth factor receptor. J. Biol. Chem. 280:13129-13136.
52. Raaijmakers, J. H., et al. 2007. The PI3K effector Arap3 interacts with the PI(3,4,5)P3 phosphatase SHIP2 in a SAM domain-dependent manner. Cell Signal. 19:1249-1257.
53. Reed, K. D., et al. 2004. The detection of monkeypox in humans in the Western Hemisphere. N. Engl. J. Med. 350:342-350.
54. Reeves, P. M., et al. 2005. Disabling poxvirus pathogenesis by inhibition of Abl-family tyrosine kinases. Nat. Med. 11:731-739.
55. Reeves, P. M., et al. 2011. Variola and monkeypox utilize conserved mechanisms of virion motility and release that depend on Abl and Src family tyrosine kinases. J. Virol. 85:21-31.
56. Rietdorf, J., et al. 2001. Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nat. Cell Biol. 3:992-1000.
57. Rimoin, A. W., et al. 2007. Endemic human monkeypox, Democratic Republic of Congo, 2001-2004. Emerg. Infect. Dis. 13:934-937.
58. Rimoin, A. W., et al. 2010. Major increase in human monkeypox incidence 30 years after smallpox vaccination campaigns cease in the Democratic Republic of Congo. Proc. Natl. Acad. Sci. U. S. A. 107:16262-16267.
59. Risco, C., et al. 2002. Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J. Virol. 76:1839-1855.
60. Roberts, K. L., and G. L. Smith. 2008. Vaccinia virus morphogenesis and dissemination. Trends Microbiol. 16:472-479.
61. Rodriguez, J. R., C. Risco, J. L. Carrascosa, M. Esteban, and D. Rodriguez. 1997. Characterization of early stages in vaccinia virus membrane biogenesis: implications of the 21-kilodalton protein and a newly identified 15-kilodalton envelope protein. J. Virol. 71:1821-1833.
62. Rohatgi, R., H. Y. Ho, and M. W. Kirschner. 2000. Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate. J. Cell Biol. 150:1299-1310.
63. Scaplehorn, N., et al. 2002. Grb2 and Nck act cooperatively to promote actin-based motility of vaccinia virus. Curr. Biol. 12:740-745.
64. Schindler, T., et al. 2000. Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 289:1938-1942.
65. Schurmans, S., et al. 1999. The mouse SHIP2 (Inppl1) gene: complementary DNA, genomic structure, promoter analysis, and gene expression in the embryo and adult mouse. Genomics 62:260-271.
66. Sleeman, M. W., et al. 2005. Absence of the lipid phosphatase SHIP2 confers resistance to dietary obesity. Nat. Med. 11:199-205.
67. Smith, G. L., A. Vanderplasschen, and M. Law. 2002. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol. 83:2915-2931.
68. Smith, K., D. Humphreys, P. J. Hume, and V. Koronakis. 2010. Enteropathogenic Escherichia coli recruits the cellular inositol phosphatase SHIP2 to regulate actin-pedestal formation. Cell Host Microbe 7:13-24.
69. Snapper, S. B., et al. 2001. N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat. Cell Biol. 3:897-904.
70. Soares, J. A., et al. 2009. Activation of the PI3K/Akt pathway early during vaccinia and cowpox virus infections is required for both host survival and viral replication. J. Virol. 83:6883-6899.
71. Sodeik, B., et al. 1993. Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks. J. Cell Biol. 121:521-541.
72. Taylor, V., et al. 2000. 5' phospholipid phosphatase SHIP-2 causes protein kinase B inactivation and cell cycle arrest in glioblastoma cells. Mol. Cell. Biol. 20:6860-6871.
73. Vandenbroere, I., N. Paternotte, J. E. Dumont, C. Erneux, and I. Pirson. 2003. The c-Cbl-associated protein and c-Cbl are two new partners of the SH2-containing inositol polyphosphate 5-phosphatase SHIP2. Biochem. Biophys. Res. Commun. 300:494-500.
74. Wang, X., E. R. Hinson, and P. Cresswell. 2007. The interferon-inducible protein viperin inhibits influenza virus release by perturbing lipid rafts. Cell Host Microbe 2:96-105.
75. Ward, B. M., and B. Moss. 2001. Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails. J. Virol. 75: 11651-11663.
76. Weisswange, I., T. P. Newsome, S. Schleich, and M. Way. 2009. The rate of N-WASP exchange limits the extent of ARP2/3-complex-dependent actinbased motility. Nature 458:87-91.
77. Wisniewski, D., et al. 1999. A novel SH2-containing phosphatidylinositol 3,4,5-trisphosphate 5-phosphatase (SHIP2) is constitutively tyrosine phosphorylated and associated with src homologous and collagen gene (SHC) in chronic myelogenous leukemia progenitor cells. Blood 93:2707-2720.
78. Xie, J., et al. 2008. The docking properties of SHIP2 influence both JIP1 tyrosine phosphorylation and JNK activity. Cell Signal. 20:1432-1441.
79. Xie, J., I. Vandenbroere, and I. Pirson. 2008. SHIP2 associates with intersectin and recruits it to the plasma membrane in response to EGF. FEBS Lett. 582:3011-3017.
80. Yu, J., et al. 2010. MicroRNA-205 promotes keratinocyte migration via the lipid phosphatase SHIP2. FASEB J. 24:3950-3959.
81. Zaborowska, I., and D. Walsh. 2009. PI3K signaling regulates rapamycininsensitive translation initiation complex formation in vaccinia virus-infected cells. J. Virol. 83:3988-3992.
82. Zhang, J., et al. 2007. SHIP2 controls PtdIns(3,4,5)P(3) levels and PKB activity in response to oxidative stress. Cell Signal. 19:2194-2200.