Enzymatically inactive US3 protein kinase of Marek's disease virus (MDV) is capable of depolymerizing F-actin but results in accumulation of virions in perinuclear invaginations and reduced virus growth

Virology

Volumn 375, Issue 1, 2008, Pages 37-47

  Schumacher, Daniel ^a   McKinney, Caleb ^a   Kaufer, Benedikt B ^a   Osterrieder, Nikolaus ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Actin; Apoptosis; Marek's disease virus; MDV; Nuclear egress; Phosphoprotein 38 (pp38); Protein kinase

Indexed keywords

ALANINE; F ACTIN; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN SERINE THREONINE KINASE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; COMPARATIVE STUDY; DEPOLYMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; MARDIVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIRION; VIROGENESIS; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS TITRATION;

ACTINS; AMINO ACID SUBSTITUTION; ANIMALS; APOPTOSIS; BINDING SITES; CELLS, CULTURED; CHICK EMBRYO; HERPESVIRUS 2, GALLID; MICROSCOPY, ELECTRON, TRANSMISSION; MUTAGENESIS, SITE-DIRECTED; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; VIRAL PROTEINS; VIRION;

GALLID HERPESVIRUS 2; GALLUS GALLUS;

EID: 42749096106     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.01.026     Document Type: Article

References (51)

1. Aubert M., O'Toole J., and Blaho J.A. Induction and prevention of apoptosis in human HEp-2 cells by herpes simplex virus type 1. J. Virol. 73 (1999) 10359-10370
2. Aubert M., Pomeranz L.E., and Blaho J.A. Herpes simplex virus blocks apoptosis by precluding mitochondrial cytochrome c release independent of caspase activation in infected human epithelial cells. Apoptosis 12 1 (2007) 19-35
3. Baigent S.J., Ross L.J., and Davison T.F. Differential susceptibility to Marek's disease is associated with differences in number, but not phenotype or location, of pp38+ lymphocytes. J. Gen. Virol. 79 (1998) 2795-2802
4. Bustelo X.R., Sauzeau V., and Berenjeno I.M. GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. Bioessays 29 4 (2007) 356-370
5. Calnek B.W. Marek's disease-a model for herpesvirus oncology. Crit. Rev. Microbiol. 12 4 (1986) 293-320
6. Calnek B.W. Pathogenesis of Marek's disease virus infection. Marek's Disease vol. 255 (2001), Springer, Berlin 25-55
7. Calnek B.W., Adldinger H.K., and Kahn D.E. Feather follicle epithelium: a source of enveloped and infectious cell-free herpesvirus from Marek's disease. Avian Dis. 14 2 (1970) 219-233
8. Calton C.M., Randall J.A., Adkins M.W., and Banfield B.W. The pseudorabies virus serine/threonine kinase Us3 contains mitochondrial, nuclear and membrane localization signals. Virus Genes 29 1 (2004) 131-145
9. Churchill A.E., and Biggs P.M. Agent of Marek's disease in tissue culture. Nature 215 (1967) 528-530
10. Copeland N.G., Jenkins N.A., and Court D.L. Recombineering: a powerful new tool for mouse functional genomics. Nat. Rev. Genet. 2 10 (2001) 769-779
11. de Wind N., Domen J., and Berns A. Herpesviruses encode an unusual protein-serine/threonine kinase which is nonessential for growth in cultured cells. J. Virol. 66 9 (1992) 5200-5209
12. Demmin G.L., Clase A.C., Randall J.A., Enquist L.W., and Banfield B.W. Insertions in the gG gene of pseudorabies virus reduce expression of the upstream Us3 protein and inhibit cell-to-cell spread of virus infection. J. Virol. 75 (2001) 10856-10869
13. Deruelle M., Geenen K., Nauwynck H.J., and Favoreel H.W. A point mutation in the putative ATP binding site of the pseudorabies virus US3 protein kinase prevents Bad phosphorylation and cell survival following apoptosis induction. Virus Res. 128 (2007) 65-70
14. Favoreel H.W., Van Minnebruggen G., Adriaensen D., and Nauwynck H.J. Cytoskeletal rearrangements and cell extensions induced by the US3 kinase of an alphaherpesvirus are associated with enhanced spread. Proc. Natl. Acad. Sci. U. S. A. 102 25 (2005) 8990-8995
15. Fukuchi K., Sudo M., Lee Y.S., Tanaka A., and Nonoyama M. Structure of Marek's disease virus DNA: detailed restriction enzyme map. J. Virol. 51 1 (1984) 102-109
16. Gimeno I.M., Witter R.L., Hunt H.D., Reddy S.M., Lee L.F., and Silva R.F. The pp38 gene of Marek's disease virus (MDV) is necessary for cytolytic infection of B cells and maintenance of the transformed state but not for cytolytic infection of the feather follicle epithelium and horizontal spread of MDV. J. Virol. 79 7 (2005) 4545-4549
17. Hanks S.K., Quinn A.M., and Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241 4861 (1988) 42-52
18. Ichijo K., Isogai H., Okada K., and Fujimoto Y. Initial proliferation site of Marek's disease tumor cells in the spleen. Zentralbl. Veterinarmed. B 28 3 (1981) 177-189
19. Kato A., Yamamoto M., Ohno T., Kodaira H., Nishiyama Y., and Kawaguchi Y. Identification of proteins phosphorylated directly by the Us3 protein kinase encoded by herpes simplex virus 1. J. Virol. 79 (2005) 9325-9331
20. Kingham B.F., Zelnik V., Kopacek J., Majerciak V., Ney E., and Schmidt C.J. The genome of herpesvirus of turkeys: comparative analysis with Marek's disease viruses. J. Gen. Virol. 82 (2001) 1123-1135
21. Kyhse-Andersen J. Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Methods 10 3-4 (1984) 203-209
22. Leader D.P., Deana A.D., Marchiori F., Purves F.C., and Pinna L.A. Further definition of the substrate specificity of the alpha-herpesvirus protein kinase and comparison with protein kinases A and C. Biochim. Biophys. Acta 1091 3 (1991) 426-431
23. Lee L.F., Wu P., Sui D.X., Ren D.L., Kamil J., Kung H.J., and Witter R.L. The complete unique long sequence and the overall genomic organization of the GA strain of Marek's disease virus. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 6091-6096
24. Marek J. Multiple NervenentzÅndung (Polyneuritis) bei HÅhnern. Dtsch. Tierärztl. Wochenschr. 15 (1907) 417-421
25. Morgan R.W., Cantello J.L., and McDermott C.H. Transfection of chicken embryo fibroblasts with Marek's disease virus DNA. Avian Dis. 34 2 (1990) 345-351
26. Mori I., Goshima F., Koshizuka T., Koide N., Sugiyama T., Yoshida T., Yokochi T., Kimura Y., and Nishiyama Y. The US3 protein kinase of herpes simplex virus attenuates the activation of the c-Jun N-terminal protein kinase signal transduction pathway in infected piriform cortex neurons of C57BL/6 mice. Neurosci. Lett. 351 3 (2003) 201-205
27. Mou F., Forest T., and Baines J.D. US3 of herpes simplex virus type 1 encodes a promiscuous protein kinase that phosphorylates and alters localization of lamin A/C in infected cells. J. Virol. 81 (2007) 6459-6470
28. Murata T., Goshima F., Daikoku T., Takakuwa H., and Nishiyama Y. Expression of herpes simplex virus type 2 US3 affects the Cdc42/Rac pathway and attenuates c-Jun N-terminal kinase activation. Genes Cells 5 (2000) 1017-1027
29. Nazerian K., Solomon J.J., Witter R.L., and Burmester B.R. Studies on the etiology of Marek's disease. II. Finding of a herpesvirus in cell culture. Proc. Soc. Exp. Biol. Med. 127 1 (1968) 177-182
30. Nguyen M.L., and Blaho J.A. Apoptosis during herpes simplex virus infection. Adv. Virus Res. 69 (2007) 67-97
31. Osterrieder N. Sequence and initial characterization of the U(L)10 (glycoprotein M) and U(L)11 homologous genes of serotype 1 Marek's disease virus. Arch. Virol. 144 (1999) 1853-1863
32. Osterrieder N., Kamil J.P., Schumacher D., Tischer B.K., and Trapp S. Marek's disease virus: from miasma to model. Nat. Rev. Microbiol. 4 (2006) 283-294
33. Osterrieder N., and Vautherot J.F. The genome content of Marek's disease-like viruses. In: Davison T.F., Nair V., and Pastoret P.P. (Eds). Marek's Disease (2004), Elsevier, London
34. Poon A.P., Benetti L., and Roizman B. U(S)3 and U(S)3.5 protein kinases of herpes simplex virus 1 differ with respect to their functions in blocking apoptosis and in virion maturation and egress. J. Virol. 80 (2006) 3752-3764
35. Poon A.P., Gu H., and Roizman B. ICP0 and the US3 protein kinase of herpes simplex virus 1 independently block histone deacetylation to enable gene expression. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 9993-9998
36. Poon A.P., and Roizman B. Mapping of key functions of the herpes simplex virus 1 U(S)3 protein kinase: the U(S)3 protein can form functional heteromultimeric structures derived from overlapping truncated polypeptides. J. Virol. 81 (2007) 1980-1989
37. Purves F.C., Deana A.D., Marchiori F., Leader D.P., and Pinna L.A. The substrate specificity of the protein kinase induced in cells infected with herpesviruses: studies with synthetic substrates [corrected] indicate structural requirements distinct from other protein kinases. Biochim. Biophys. Acta 889 (1986) 208-215
38. Purves F.C., Longnecker R.M., Leader D.P., and Roizman B. Herpes simplex virus 1 protein kinase is encoded by open reading frame US3 which is not essential for virus growth in cell culture. J. Virol. 61 (1987) 2896-2901
39. Purves F.C., Spector D., and Roizman B. The herpes simplex virus 1 protein kinase encoded by the US3 gene mediates posttranslational modification of the phosphoprotein encoded by the UL34 gene. J. Virol. 65 (1991) 5757-5764
40. Purves F.C., Spector D., and Roizman B. UL34, the target of the herpes simplex virus U(S)3 protein kinase, is a membrane protein which in its unphosphorylated state associates with novel phosphoproteins. J. Virol. 66 (1992) 4295-4303
41. Reddy S.M., Lupiani B., Gimeno I.M., Silva R.F., Lee L.F., and Witter R.L. Rescue of a pathogenic Marek's disease virus with overlapping cosmid DNAs: use of a pp38 mutant to validate the technology for the study of gene function. Proc. Natl. Acad. Sci. U.S.A. 99 10 (2002) 7054-7059
42. Reynolds A.E., Ryckman B.J., Baines J.D., Zhou Y., Liang L., and Roller R.J. U(L)31 and U(L)34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids. J. Virol. 75 (2001) 8803-8817
43. Ryckman B.J., and Roller R.J. Herpes simplex virus type 1 primary envelopment: UL34 protein modification and the US3-UL34 catalytic relationship. J. Virol. 78 (2004) 399-412
44. Sambrook J., and Maniatis T. Molecular Cloning: a Laboratory Manual (1989), Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
45. Schumacher D., Tischer B.K., Fuchs W., and Osterrieder N. Reconstitution of Marek's disease virus serotype 1 (MDV-1) from DNA cloned as a bacterial artificial chromosome and characterization of a glycoprotein B-negative MDV-1 mutant. J. Virol. 74 (2000) 11088-11098
46. Schumacher D., Tischer B.K., Trapp S., and Osterrieder N. The protein encoded by the US3 orthologue of Marek's disease virus is required for efficient de-envelopment of perinuclear virions and involved in actin stress fiber breakdown. J. Virol. 79 (2005) 3987-3997
47. Shek W.R., Calnek B.W., Schat K.A., and Chen C.H. Characterization of Marek's disease virus-infected lymphocytes: discrimination between cytolytically and latently infected cells. J. Natl. Cancer Inst. 70 (1983) 485-491
48. Tischer B.K., von Einem J., Kaufer B., and Osterrieder N. Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques 40 (2006) 191-197
49. Tulman E.R., Afonso C.L., Lu Z., Zsak L., Rock D.L., and Kutish G.F. The genome of a very virulent Marek's disease virus. J. Virol. 74 (2000) 7980-7988
50. Valderrama F., Cordeiro J.V., Schleich S., Frischknecht F., and Way M. Vaccinia virus-induced cell motility requires F11L-mediated inhibition of RhoA signaling. Science 311 (2006) 377-381
51. Van Minnebruggen G., Favoreel H.W., Jacobs L., and Nauwynck H.J. Pseudorabies virus US3 protein kinase mediates actin stress fiber breakdown. J. Virol. 77 (2003) 9074-9080