Home LiteratureArticle Details
PMID: 8627658 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Human cytomegalovirus carries serine/threonine protein phosphatases PP1 and a host-cell derived PP2A.

Journal of virology ·Vol. 70 ·No. 3 ·1996-03-00 ·Pages 1415-23

Michelson S, Turowski P, Picard L, Goris J, Landini MP, Topilko A, Hemmings B, Bessia C, Garcia A, Virelizier JL

Abstract

Human cytomegalovirus (CMV), a herpesvirus, is an important cause of morbidity and mortality in immunocompromised patients. When studying hyper-immediate-early events after contact between CMV virions and the cell membrane, we observed a hypophosphorylation of cellular proteins within 10 min. This can be explained in part by our finding that purified CMV contains serine/threonine protein phosphatase activities. Biochemical analyses indicate that this protein phosphatase activity has all characteristics of type 1 and 2A protein phosphatases (PP1 and PP2A). Specifically, PP1 accounts for approximately 30% and PP2A accounts for the remaining 70% of the phosphorylase phosphatase activity found. CMV produced in astrocytoma cells stably expressing an amino-terminally tagged PP2A catalytic subunit contained tagged enzyme, thus demonstrating the cellular origin of CMV-associated PP2A. PP2A is specifically found inside the virus, associated with the nucleocapsid fraction. Western blot (immunoblot) analysis of purified virus revealed the presence of the catalytic subunits of PP2A and PP1. Furthermore, the catalytic subunit of PP2A appears to be complexed to the regulatory subunits PR65 and PR55, which is also the most abundant configuration of this enzyme found in the host cells. Incubation of virus with okadaic acid before contact of CMV with cells prevented hypophosphorylation of cellular proteins, thus demonstrating the role of CMV-associated phosphatases in this phenomenon. CMV can thus transport an active enzyme from one cell to another.

MeSH Terms
Amino Acid Sequence Cell Line Cytomegalovirus/enzymology,ultrastructure Humans Molecular Sequence Data Phosphoprotein Phosphatases/antagonists & inhibitors,metabolism Phosphorylation Tumor Cells, Cultured Virion/metabolism
Chemicals
Phosphoprotein Phosphatases
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Michelson S
Unité d'Immunologie Virale, Institut Pasteur, Paris, France.
Turowski P
Picard L
Goris J
Landini M P
Topilko A
Hemmings B
Bessia C
Garcia A
Virelizier J L
References (50)
50 references, click to expand
  1. The 55 kd regulatory subunit of Drosophila protein phosphatase 2A is required for anaphase.
    Cell. 1993 Feb 26;72(4):621-33 PMID: 8382567
  2. Protein phosphatases in cell signalling.
    Curr Opin Cell Biol. 1992 Dec;4(6):1000-7 PMID: 1336668
  3. Analysis of subunit isoforms in protein phosphatase 2A holoenzymes from rabbit and Xenopus.
    J Biol Chem. 1993 Apr 5;268(10):7330-7 PMID: 7681822
  4. A protein phosphatase related to the vaccinia virus VH1 is encoded in the genomes of several orthopoxviruses and a baculovirus.
    Proc Natl Acad Sci U S A. 1993 May 1;90(9):4017-21 PMID: 8387208
  5. Structure and expression of a 72-kDa regulatory subunit of protein phosphatase 2A. Evidence for different size forms produced by alternative splicing.
    J Biol Chem. 1993 Jul 15;268(20):15267-76 PMID: 8392071
  6. On target with a new mechanism for the regulation of protein phosphorylation.
    Trends Biochem Sci. 1993 May;18(5):172-7 PMID: 8392229
  7. Induction of endogenous human cytomegalovirus gene expression after differentiation of monocytes from healthy carriers.
    J Virol. 1994 Mar;68(3):1597-604 PMID: 8107221
  8. Hyperimmediate entry of human cytomegalovirus virions and dense bodies into human fibroblasts.
    Res Virol. 1994 Mar-Apr;145(2):75-82 PMID: 8059068
  9. Molecular cloning of cDNA encoding the 110 kDa and 21 kDa regulatory subunits of smooth muscle protein phosphatase 1M.
    FEBS Lett. 1994 Dec 12;356(1):51-5 PMID: 7988720
  10. Human cytomegalovirus structural proteins.
    J Gen Virol. 1994 Dec;75 ( Pt 12):3287-308 PMID: 7527833
  11. Nuclear targeting of the tegument protein pp65 (UL83) of human cytomegalovirus: an unusual bipartite nuclear localization signal functions with other portions of the protein to mediate its efficient nuclear transport.
    J Virol. 1995 Feb;69(2):1071-8 PMID: 7815485
  12. Differential methylation and altered conformation of cytoplasmic and nuclear forms of protein phosphatase 2A during cell cycle progression.
    J Cell Biol. 1995 Apr;129(2):397-410 PMID: 7721943
  13. Host cellular annexin II is associated with cytomegalovirus particles isolated from cultured human fibroblasts.
    J Virol. 1995 Aug;69(8):4784-91 PMID: 7609045
  14. Human cytomegalovirus: glycoproteins associated with virions and dense bodies.
    J Virol. 1976 Aug;19(2):594-609 PMID: 183016
  15. Requirement of protein synthesis for the degradation of host mRNA in Friend erythroleukemia cells infected wtih herpes simplex virus type 1.
    J Virol. 1978 Sep;27(3):619-27 PMID: 212585
  16. Human cytomegalovirus-associated DNA polymerase and protein kinase activities.
    J Gen Virol. 1981 Nov;57(Pt 1):149-56 PMID: 6275014
  17. Complete primary structure of protein phosphatase inhibitor-1 from rabbit skeletal muscle.
    Eur J Biochem. 1982 Aug;126(2):235-46 PMID: 6290217
  18. A DNA-nicking activity associated with the nucleocapsid of human cytomegalovirus.
    Arch Virol. 1982;73(3-4):351-6 PMID: 6293419
  19. Properties of a Mr = 38,000 phosphoprotein phosphatase. Modulation by divalent cations, ATP, and fluoride.
    J Biol Chem. 1983 Apr 10;258(7):4214-9 PMID: 6300079
  20. Vaccinia virus induces cellular mRNA degradation.
    J Virol. 1983 Sep;47(3):529-39 PMID: 6620463
  21. Regulation of protein phosphatase activity by the deinhibitor protein.
    Adv Enzyme Regul. 1984;22:467-84 PMID: 6089515
  22. Catalytic properties of a human cytomegalovirus-induced protein kinase.
    Eur J Biochem. 1985 Jun 3;149(2):393-9 PMID: 2986975
  23. Characterization of phosphoproteins and protein kinase activity of virions, noninfectious enveloped particles, and dense bodies of human cytomegalovirus.
    J Virol. 1986 Sep;59(3):714-27 PMID: 3016333
  24. Purification and properties of polycation-stimulated phosphorylase phosphatases from rabbit skeletal muscle.
    J Biol Chem. 1987 Jan 25;262(3):1049-59 PMID: 3027074
  25. The product of the mei3+ gene, expressed under control of the mating-type locus, induces meiosis and sporulation in fission yeast.
    EMBO J. 1987 Mar;6(3):729-36 PMID: 3034608
  26. Molecular cloning of cDNAs encoding two isoforms of the catalytic subunit of protein phosphatase 2A.
    Biochemistry. 1987 Nov 17;26(23):7215-20 PMID: 2827745
  27. Stimulation of the ATP, Mg-dependent protein phosphatase by p-nitrophenyl phosphate.
    Anal Biochem. 1988 Jun;171(2):423-8 PMID: 2841890
  28. Isolation of an active form of the ATP + Mg2+-dependent protein phosphatase stimulated by the deinhibitor protein and by p-nitrophenyl phosphate.
    Biochem J. 1988 Sep 1;254(2):501-7 PMID: 2845955
  29. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics.
    Biochem J. 1988 Nov 15;256(1):283-90 PMID: 2851982
  30. An improved procedure for identifying and quantitating protein phosphatases in mammalian tissues.
    FEBS Lett. 1989 Jul 3;250(2):596-600 PMID: 2546812
  31. The structure and regulation of protein phosphatases.
    Annu Rev Biochem. 1989;58:453-508 PMID: 2549856
  32. Identification of the ATP + Mg-dependent and polycation-stimulated protein phosphatases in the germinal vesicle of the Xenopus oocyte.
    Biochem J. 1989 May 15;260(1):45-51 PMID: 2549958
  33. Activation of proto-oncogenes: an immediate early event in human cytomegalovirus infection.
    Science. 1990 Feb 2;247(4942):561-4 PMID: 1689075
  34. Okadaic acid: a new probe for the study of cellular regulation.
    Trends Biochem Sci. 1990 Mar;15(3):98-102 PMID: 2158158
  35. Three forms of phosphatase type 1 in Swiss 3T3 fibroblasts. Free catalytic subunit appears to mediate s6 dephosphorylation.
    J Biol Chem. 1990 Dec 25;265(36):22460-6 PMID: 2176218
  36. Identification of members of the protein phosphatase 1 gene family in the rat and enhanced expression of protein phosphatase 1 alpha gene in rat hepatocellular carcinomas.
    Jpn J Cancer Res. 1990 Dec;81(12):1272-80 PMID: 2177460
  37. Protein phosphatases: recent progress.
    Adv Second Messenger Phosphoprotein Res. 1991;23:1-121 PMID: 1847640
  38. A Tyr/Ser protein phosphatase encoded by vaccinia virus.
    Nature. 1991 Mar 28;350(6316):359-62 PMID: 1848923
  39. Classification of protein-serine/threonine phosphatases: identification and quantitation in cell extracts.
    Methods Enzymol. 1991;201:389-98 PMID: 1658556
  40. Protein phosphatases and DNA tumor viruses: transformation through the back door?
    Cell Regul. 1991 Aug;2(8):589-98 PMID: 1663787
  41. Characterization of the interaction of polyomavirus middle T antigen with type 2A protein phosphatase.
    J Virol. 1992 Mar;66(3):1458-67 PMID: 1371166
  42. Receptor-initiated activation of cells and their oncogenes by herpes-family viruses.
    J Invest Dermatol. 1992 Jun;98(6 Suppl):29S-35S PMID: 1316926
  43. Human cytomegalovirus contains a tegument protein that enhances transcription from promoters with upstream ATF and AP-1 cis-acting elements.
    J Virol. 1992 Jul;66(7):4434-44 PMID: 1318413
  44. The human fibroblast receptor for gp86 of human cytomegalovirus is a phosphorylated glycoprotein.
    J Virol. 1992 Aug;66(8):4834-8 PMID: 1321272
  45. NH2-terminal modification of the phosphatase 2A catalytic subunit allows functional expression in mammalian cells.
    J Biol Chem. 1992 Aug 25;267(24):16883-8 PMID: 1380955
  46. Nuclear protein phosphorylation and growth control.
    Biochem J. 1992 Oct 1;287 ( Pt 1):1-15 PMID: 1417761
  47. The 55 kDa regulatory subunit of protein phosphatase 2A plays a role in the activation of the HPV16 long control region in human cells with a deletion in the short arm of chromosome 11.
    EMBO J. 1992 Dec;11(12):4601-6 PMID: 1330540
  48. Human cytomegalovirus infection of the major leukocyte subpopulations and evidence for initial viral replication in polymorphonuclear leukocytes from viremic patients.
    J Infect Dis. 1992 Dec;166(6):1236-44 PMID: 1331248
  49. The lower matrix protein pp65 is the principal viral antigen present in peripheral blood leukocytes during an active cytomegalovirus infection.
    J Gen Virol. 1992 Nov;73 ( Pt 11):2923-32 PMID: 1331294
  50. PPX, a novel protein serine/threonine phosphatase localized to centrosomes.
    EMBO J. 1993 Mar;12(3):987-96 PMID: 8384557
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1996-03-00
Pages
1415-23
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC189961
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com