DOI: 10.1111/j.1432-1033.1997.t01-1-00200.x. Modulation of the Enzymatic Properties of Protein Phosphatase 2A Catalytic Subunit by the Recombinant 65‐kDa Regulatory Subunit PR65α

Modulation of the Enzymatic Properties of Protein Phosphatase 2A Catalytic Subunit by the Recombinant 65‐kDa Regulatory Subunit PR65α

10.1111/j.1432-1033.1997.t01-1-00200.x

Crossref journal-article

Wiley

European Journal of Biochemistry (311)

Abstract

All protein phosphatase 2A (PP2A) holoenzymes contain a 36‐kDa catalytic subunit (PP2Ac) and a regulatory subunit of 6.5 kDa (PR6.5). We have studied the interaction between PP2Ac and PR65 in an in vitro system, using PP2Ac isolated from rabbit skeletal muscle and recombinant PR6Sa expressed in bacteria or insect cells. Bacterially expressed PR6Sa exhibited identical biochemical properties to the protein expressed and isolated from the baculoviral expression system. The association of recombinant PR6.5 with PP2Ac was very tight (KappD= 85 pM) and led to a suppression of PP2A activity, which was maximal (70–80 %) when phosphoproteins were used as substrates. When less‐structured or smaller substrates (such as phosphopeptides) were used, this inhibition was only 30 %. PR6.5 stimulated PP2Ac activity when the assays were performed in the presence of polycations. This indicates that the PR6.5 not only serves the previously predicted structural role as a molecular scaffold, but also allosterically modulates the enzymatic properties of PP2Ac. Furthermore, we identified a site of interaction between PP2Ac and PR6Sα by disruption of a stretch of basic amino acids by introduction of a glutamate at position 416. This produced an almost 100‐fold reduced affinity for PP2Ac and indicated that this basic motif is an important determinant for the interaction of PR6.5 and PP2Ac.

Bibliography

Turowski, P., Favre, B., Campbell, K. S., Lamb, N. J. C., & Hemmings, B. A. (1997). Modulation of the Enzymatic Properties of Protein Phosphatase 2A Catalytic Subunit by the Recombinant 65âkDa Regulatory Subunit PR65Î±. European Journal of Biochemistry, 248(1), 200â208. Portico.

Authors 5

Patric Turowski (first)
Bertrand Favre (additional)
Kathryn S. Campbell (additional)
Ned J. C. Lamb (additional)
Brian A. Hemmings (additional)

References 52 Referenced 58

10.1016/S0065-3233(08)60245-4
10.1111/j.1432-1033.1990.tb15482.x
10.1111/j.1432-1033.1992.tb16774.x
10.1002/elps.1150080203
10.1016/S0021-9258(19)83888-7 / J. Biol. Chem. / Dephosphorylation of CAMP‐dependent protein kinase regulatory subunit (type 11) by calmodulin‐dependent protein phosphatase by Blumenthal D. K. (1986)
10.1111/j.1432-1033.1995.1037g.x
10.1002/j.1460-2075.1993.tb05739.x
10.1128/jvi.69.6.3721-3728.1995 / J. virol. / Identification of regions in polyomavirus middle T and small T antigens important for association with protein phosphatase 2A by Campbell K. S. (1995)
10.1016/S0021-9258(18)83230-6 / J. Biol. Chem. / Isolation and partial characterization of an M, 60000 subunit of a type 2A phosphatase from rabbit reticulocytes by Chen S.‐C. (1989)
10.1016/0076-6879(83)99059-6
10.1016/0076-6879(88)59039-0
10.1146/annurev.bi.58.070189.002321
10.1016/0014-5793(90)81285-V
10.1016/0003-9861(81)90505-1
10.1074/jbc.271.5.2578
{'key': 'e_1_2_2_17_1', 'first-page': '109', 'article-title': 'Dephosphorylation of phosphopeptides by calcineurin (protein phosphatase 2B), Eur:', 'volume': '219', 'author': 'Donella‐Deana A.', 'year': '1994', 'journal-title': 'J. Biochem.'} / J. Biochem. / Dephosphorylation of phosphopeptides by calcineurin (protein phosphatase 2B), Eur: by Donella‐Deana A. (1994)
10.1016/S0021-9258(17)34009-7
10.1038/376745a0
10.1016/0092-8674(95)90439-5
10.1016/B978-0-12-152821-8.50009-8
{'key': 'e_1_2_2_22_1', 'first-page': '473', 'article-title': 'Phosphorylation of the type‐I1 regulatory subunit of cyclic‐AMP‐dependent protein kinase by glycogen synthase kinase 3 and glycogen synthase kinase 5, Eur', 'volume': '127', 'author': 'Hemmings B. A.', 'year': '1982', 'journal-title': 'J. Biochem.'} / J. Biochem. / Phosphorylation of the type‐I1 regulatory subunit of cyclic‐AMP‐dependent protein kinase by glycogen synthase kinase 3 and glycogen synthase kinase 5, Eur by Hemmings B. A. (1982)
10.1021/bi00465a002
10.1016/S0021-9258(18)53179-3 / Xenopus, J. Biol. Chem. / Analysis of subunit isoforms in protein phosphatase 2A holoenzymes from rabbit and by Hendrix P. (1993)
10.1016/0301-4622(90)80043-7
10.1016/S0021-9258(19)36692-X / J. Biol. Chem. / Expression of the A subunit of protein phosphatase 2A and characterization of its interaction with the catalytic and regulatory subunits by Kamibayashi C. (1992)
10.1073/pnas.72.9.3448
10.1021/ac00125a006
10.1038/227680a0
10.1016/0092-8674(91)90124-H
10.1242/jcs.107.9.2609 / J. Cell Sci. / Drosophila mutants in the 55 kDa regulatory subunit of protein phosphatase 2A show strongly reduced ability to dephosphorylate substrates of p34,cdc2 by Mayer‐Jaekel R. E. (1994)
10.1016/0962-8924(94)90219-4
10.1002/j.1460-2075.1987.tb04814.x
{'key': 'e_1_2_2_34_1', 'first-page': '689', 'article-title': 'Protein phosphatases and DNA tumor viruses: transformation through the back door?', 'volume': '211', 'author': 'Mumby M. C.', 'year': '1991', 'journal-title': 'Cell Regul. 2, Biophys.'} / Cell Regul. 2, Biophys. / Protein phosphatases and DNA tumor viruses: transformation through the back door? by Mumby M. C. (1991)
10.1152/physrev.1993.73.4.673
10.1016/0167-4889(94)90050-7
10.1128/MCB.12.11.4872
10.1128/JVI.68.1.123-129.1994
10.1016/0926-6585(66)90333-5
10.1021/bi00397a003
{'key': 'e_1_2_2_41_1', 'first-page': '1', 'article-title': 'A manual of methods for baculovirus vectors and insect cell culture procedures', 'volume': '1555', 'author': 'Summers M. D.', 'year': '1987', 'journal-title': 'Texas Agric. Exp. Stn Bull.'} / Texas Agric. Exp. Stn Bull. / A manual of methods for baculovirus vectors and insect cell culture procedures by Summers M. D. (1987)
10.1042/bj2750233
10.1016/S0021-9258(19)62316-1 / J. Biol. Chem. / Site‐specific phosphorylation of beta‐casein by protein kinases from rabbit reticulocytes by Tuazon P. T. (1978)
10.1111/j.1432-1033.1979.tb12918.x
10.1111/j.1432-1033.1985.tb08833.x
10.1083/jcb.129.2.397
10.1073/pnas.86.10.3584
10.1016/S0021-9258(19)75748-2 / J. Biol. Chem. / Purification and properties of polycation‐stimulated phophorylase phosphatase from rabbit skeletal muscle by Waelkens E. (1987)
10.1017/S0022029900028429
10.1074/jbc.270.36.21374
10.1042/bj3110017
10.1016/0076-6879(79)63019-7
10.1042/bj3170187

Dates

Type	When
Created	21 years, 1 month ago (July 16, 2004, 5:46 a.m.)
Deposited	1 year, 9 months ago (Nov. 22, 2023, 4:11 p.m.)
Indexed	3 months, 3 weeks ago (May 3, 2025, 6:44 p.m.)
Issued	28 years ago (Aug. 1, 1997)
Published	28 years ago (Aug. 1, 1997)
Published Online	21 years, 1 month ago (July 16, 2004)
Published Print	28 years ago (Aug. 1, 1997)

Funders 0

None

BibTeX

@article{Turowski_1997, title={Modulation of the Enzymatic Properties of Protein Phosphatase 2A Catalytic Subunit by the Recombinant 65‐kDa Regulatory Subunit PR65α}, volume={248}, ISSN={1432-1033}, url={http://dx.doi.org/10.1111/j.1432-1033.1997.t01-1-00200.x}, DOI={10.1111/j.1432-1033.1997.t01-1-00200.x}, number={1}, journal={European Journal of Biochemistry}, publisher={Wiley}, author={Turowski, Patric and Favre, Bertrand and Campbell, Kathryn S. and Lamb, Ned J. C. and Hemmings, Brian A.}, year={1997}, month=aug, pages={200–208} }

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