Brain protein phosphatase 2A: Developmental regulation and distinct cellular and subcellular localization by B subunits

Journal of Comparative Neurology

Volumn 392, Issue 4, 1998, Pages 515-527

  Strack, Stefan ^a,b   Zaucha, Julie A ^a   Ebner, Ford F ^b   Colbran, Roger J ^a,b   Wadzinski, Brian E ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

Cell compartmentation; Immunohistochemistry; Phosphorylation; Signal transduction; Subcellular fractions

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE 2A;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELLULAR DISTRIBUTION; ENZYME LOCALIZATION; GROWTH REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODY SPECIFICITY; BRAIN; CELL COMPARTMENTATION; COS CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IMMUNOHISTOCHEMISTRY; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS;

EID: 0032536810     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980323)392:4<515::AID-CNE8>3.0.CO;2-3     Document Type: Article

References (66)

1. Akiyama, N., H. Shima, Y. Hatano, Y. Osawa, T. Sugimura, and M. Nagao (1995) cDNA cloning of BR gamma, a novel brain-specific isoform of the B regulatory subunit of type-2A protein phosphatase. Eur. J. Biochem. 230:766-772.
2. Barnes, G.N., J.T. Slevin, and T.C. Vanaman (1995) Rat brain protein phosphatase 2A: An enzyme that may regulate autophosphorylated protein kinases. J. Neurochem. 64:340-353.
3. Beverley, S.M. (1995) Enzymatic amplification of RNA by PCR. In F.M. Ausubel, R. Brent, R.E. Kingston, et al. (eds): Current Protocols in Molecular Biology. New York: Wiley-Liss, Inc., pp. 15.14.11-15.14.16.
4. Bollen, M. and W. Stalmans (1992) The structure, role, and regulation of type 1 protein phosphatases. Crit. Rev. Biochem. Mol. Biol. 27:227-281.
5. Brautigan, D.L. (1994) Protein phosphatases. Rec. Progr. Hormone Res. 49:197-214.
6. Cohen, P. (1989) The structure and regulation of protein phosphatases. Annu. Rev. Biochem. 58:453-508.
7. Cohen, P. (1991) Classification of protein-serine/threonine phosphatases: Identification and quantitation in cell extracts. Methods Enzymol. 201:389-398.
8. Colbran, R.J., M.A. Bass, R.B. McNeill, M. Bollen, S. Zhao, B.E. Wadzinski, and S. Strack (1997) Association of brain protein phosphatase 1 with cytoskeletal targeting/regulatory subunits. J. Neurochem. 69:920-929.
9. Csortos, C., S. Zolnierowicz, E. Bako, S.D. Durbin, and A.A. DePaoli-Roach (1996) High complexity in the expression of the B′ subunit of protein phosphatase 2A0. Evidence for the existence of at least seven novel isoforms. J. Biol. Chem. 271:2578-2588.
10. da Cruz e Silva, E.F., C.A. Fox, C.C. Ouimet, E. Gustafson, S.J. Watson, and P. Greengard (1995) Differential expression of protein phosphatase 1 isoforms in mammalian brain. J. Neurosci. 15:3375-3389.
11. DePaoli-Roach,A.A., I.-K. Park, V. Cerovsky, C. Csortos, S.D. Durbin, M.J. Kuntz, A. Sitikov, P.M. Tang, A. Verin, and S. Zolnierowicz (1994) Serine/threonine protein phosphatases in the control of cell function. Adv. Enzyme Regul. 34:199-224.
12. Dudek, SM. and G.V.W. Johnson (1995) Postnatal changes in serine/ threonine protein phosphatases and their association with microtubules. Brain Res. Dev. Brain Res. 90:54-61.
13. Faux, M.C. and J.D. Scott (1996) Molecular glue: Kinase anchoring and scaffold proteins. Cell 85:9-12.
14. Finney, M. (1995) Molecular cloning of PCR products. In F.M. Ausubel, R. Brent, R.E. Kingston, et al. (eds): Current Protocols in Molecular Biology. New York: Wiley-Liss, Inc., pp. 15.17.11-15.17.13.
15. Gilman, M. (1995) Ribonuclease protection assay. In F.M. Ausubel, R. Brent, R.E. Kingston, et al. (eds): Current Protocols in Molecular Biology. New York: Wiley-Liss, Inc., pp. 4.7.1-4.7.3.
16. Gong, C.X., S. Shaikh, J.Z. Wang, T. Zaidi, I. Grundke-Iqbal, and K. Iqbal (1995) Phosphatase activity toward abnormally phosphorylated tau: Decrease in Alzheimer disease brain. J. Neurochem. 65:732-738.
17. Goto, S., Y. Matsukado, Y. Mihara, N. Inoue, and E. Miyamoto (1986) The distribution of calcineurin in rat brain by light and electron microscopic immunohistochemistry and enzyme-immunoassay. Brain Res. 397:161-172.
18. Harlow, E., and D.P. Lane (1988) Antibodies: A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
19. Hatano, Y., H. Shima, T. Haneji, A.B. Miura, T. Sugimura, and M. Nagao (1993) Expression of PP2A B regulatory subunit beta isotype in rat testis. FEBS Lett. 324:71-75.
20. Hemmings, B.A., C. Adams-Pearson, F. Maurer, P. Muller, J. Goris, W. Merlevede, J. Hofsteenge, and S.R. Stone (1990) Alpha-and beta-forms of the 65-kDa subunit of protein phosphatase 2A have a similar 39 amino acid repeating structure. Biochemistry 29:3166-3173.
21. Hendrix, P., R.E. Mayer-Jackel, P. Cron, J. Goris, J. Hofsteenge, W. Merlevede, and B.A. Hemmings (1993) 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. 268:15267-15276.
22. Hubbard, M.J. and P. Cohen (1993) On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18:172-177.
23. Ingebritsen, T.S. and P. Cohen (1983) The protein phosphatases involved in cellular regulation. 1. Classification and substrate specificities. Eur. J. Biochem. 132:255-261.
24. Kamibayashi, C., R. Estes, R.L. Lickteig, S.I. Yang, C. Craft, and M.C. Mumby (1994) Comparison of heterotrimeric protein phosphatase 2A containing different B subunits. J. Biol. Chem. 269:20139-20148.
25. Khew-Goodall, Y. and B.A. Hemmings (1988) Tissue-specific expression of mRNAs encoding alpha-and beta-catalytic subunits of protein phosphatase 2A. FEBS Lett. 238:265-268.
26. Kingston, R.E. (1995) CsCl purification of RNA from tissue. In F.M. Ausubel, R. Brent, R.E. Kingston, et al. (eds): Current Protocols in Molecular Biology. New York: Wiley-Liss, Inc., pp. 4.2.5-4.2.7.
27. Krueger, K.M., Y. Daaka, J.A. Pitcher, and R.J. Lefkowitz (1997) The role of sequestration in G protein-coupled receptor resensitization. Regulation of beta2-adrenergic receptor dephosphorylation by vesicular acidification. J. Biol. Chem. 272:5-8.
28. Kuno, T., H. Mukai, A. Ito, C.D. Chang, K. Kishima, N. Saito, and C. Tanaka (1992) Distinct cellular expression of calcineurin A alpha and A beta in rat brain. J. Neurochem. 58:1643-1651.
29. Le Romancer, M., F. Reyl-Desmars, Y. Cherifi, C. Pigeon, S. Bottari, O. Meyer, and M.J. Lewin (1994) The 86-kDa subunit of autoantigen Ku is a somatostatin receptor regulating protein phosphatase-2A activity. J. Biol. Chem. 269:17464-17468.
30. Mayer, R.E., P. Hendrix, P. Cron, R. Matthies, S.R. Stone, J. Goris, W. Merlevede, J. Hofsteenge, and B.A. Hemmings (1991) Structure of the 55-kDa regulatory subunit of protein phosphatase 2A: Evidence for a neuronal-specific isoform. Biochemistry 30:3589-3597.
31. Mayer-Jaekel, R.E. and B.A. Hemmings (1995) Role of protein phosphatase 2A in Drosophila development. Semin. Cancer Biol. 6:249-256.
32. Mayer-Jaekel, R.E., H. Ohkura, P. Ferrigno, N. Andjelkovic, K. Shiomi, T. Uemura, D.M. Glover, and B.A. Hemmings (1994) Drosophila mutants in the 55 kDa regulatory subunit of protein phosphatase 2A show strongly reduced ability to dephosphorylate substrates of p34cdc2. J. Cell Sci. 107:2609-2616.
33. McCright, B. and D.M. Virshup (1995) Identification of a new family of protein phosphatase 2A regulatory subunits. J. Biol. Chem. 270:26123-26128.
34. McCright, B., A.M. Rivers, S. Audlin, and D.M. Virshup (1996) The B56 family of protein phosphatase 2A (PP2A) regulatory subunits encodes differentiation-induced phosphoproteins that target PP2A to both nucleus and cytoplasm. J. Biol. Chem. 271:22081-22089.
35. 2+/calmodulin-dependent protein kinase II with neuronal cytoskeletal proteins. Characterization of binding to a 190-kDa postsynaptic density protein. J. Biol. Chem. 270:10043-10049.
36. Moorhead, G., R.W. MacKintosh, N. Morrice, T. Gallagher, and C. MacKintosh (1994) Purification of type 1 protein (serine/threonine) phosphatases by microcystin-Sepharose affinity chromatography. FEBS Lett. 356:46-50.
37. Moorhead, G., C. MacKintosh, N. Morrice, and P. Cohen (1995) Purification of the hepatic glycogen-associated form of protein phosphatase-1 by microcystin-Sepharose affinity chromatography. FEBS Lett. 362:101-105.
38. Mulkey, R.M., C.E. Herron, and R.C. Malenka (1993) An essential role for protein phosphatases in hippocampal long-term depression. Science 261:1051-1055.
39. Mulkey, R.M., S. Endo, S. Shenolikar, and R.C. Malenka (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369:486-488.
40. Mumby, M.C. and G. Walter (1993) Protein serine/threonine phosphatases: Structure, regulation, and functions in cell growth. Physiol. Rev. 73:673-699.
41. Nairn, A.C. and S. Shenolikar (1992) The role of protein phosphatases in synaptic transmission, plasticity and neuronal development. Curr. Opin. Neurobiol. 2:296-301.
42. Ouimet, C.C., E.F. da Cruz e Silva, and P. Greengard (1995) The alpha and gamma 1 isoforms of protein phosphatase 1 are highly and specifically concentrated in dendritic spines. Proc. Natl. Acad. Sci. USA 92:3396-3400.
43. Saito, T., H. Shima, Y. Osawa, M. Nagao, B.A. Hemmings, T. Kishimoto, and S. Hisanaga (1995) Neurofilament-associated protein phosphatase 2A: Its possible role in preserving neurofilaments in filamentous states. Biochemistry 34:7376-7384.
44. Saitoh, Y., H. Yamamoto, Y. Ushio, and E. Miyamoto (1989) Characterization of polyclonal antibodies to brain protein phosphatase 2A and immunohistochemical localization of the enzyme in rat brain. Brain Res. 489:291-301.
45. Selden, R.F. (1996) Transfection using DEAE-dextran. In F.M. Ausubel, R. Brent, R.E. Kingston, et al. (eds): Current Protocols in Molecular Biology. New York: Wiley-Liss, Inc., pp. 9.2.1-9.2.6.
46. Shenolikar, S. (1994) Protein serine/threonine phosphatases-New avenues for cell regulation. Annu. Rev. Cell Biol. 10:55-86.
47. Shiomi, K., M. Takeichi, Y. Nishida, Y. Nishi, and T. Uemura (1994) Alternative cell fate choice induced by low-level expression of a regulator of protein phosphatase 2A in the Drosophila peripheral nervous system. Development 120:1591-1599.
48. Sim, A.T. (1991) The regulation and function of protein phosphatases in the brain. Mol. Neurobiol. 5:229-246.
49. Sim, A.T., E. Ratcliffe, M.C. Mumby, E. Villa-Moruzzi, and J.A. Rostas (1994) Differential activities of protein phosphatase types 1 and 2A in cytosolic and particulate fractions from rat forebrain. J. Neurochem. 62:1552-1559.
50. Sontag, E., V. Nunbhakdi-Craig, O.S. Bloom, and M.C. Mumby (1995) A novel pool of protein phosphatase 2A is associated with microtubules and is regulated during the cell cycle. J. Cell Biol. 128:1131-1144.
51. Sontag, E., V. Nunbhakdi-Craig, G. Lee, G.S. Bloom, and M.C. Mumby (1996) Regulation of the phosphorylation state and microtubulebinding activity of Tau by protein phosphatase 2A. Neuron 17:1201-1207.
52. Stone, S.R., J. Hofsteenge, and B.A. Hemmings (1987) Molecular cloning of cDNAs encoding two isoforms of the catalytic subunit of protein phosphatase 2A. Biochemistry 26:7215-7220.
53. Strack, S., B.E. Wadzinski, and F.F. Ebner (1996) Localization of the calcium/calmodulin-dependent protein phosphatase, calcineurin, in the hindbrain and spinal cord of the rat. J. Comp. Neurol. 375:66-76.
54. ++/ calmodulin-dependent protein kinase II by protein phosphatases type 1 and 2A. J. Neurochem. 68-2119-2118.
55. Strack, S., S. Choi, D.M. Lovinger, and R.J. Colbran (1997b) Translocation of autophosphorylated calcium/calmodulin-dependent protein kinase II to the postsynaptic density. J. Biol. Chem. 272:13467-13470.
56. Strack, S., R.S. Westphal, R.J. Colbran, F.F. Ebner, and B.E. Wadzinski (1997c) Protein serine/threonine phosphatase 1 and 2A associate with and dephosphorylate neurofilaments. Brain Res. Mol. Brain Res. 49:15-28.
57. Tanabe, O., T. Nagase, T. Murakami, H. Nozaki, H. Usui, Y. Nishito, H. Hayashi, H. Kagamiyama, and M. Takeda (1996) Molecular cloning of a 74-kDa regulatory subunit (B″ or delta) of human protein phosphatase 2A. FEBS Lett. 379:107-111.
58. Tehrani, M.A., M.C. Mumby, and C. Kamibayashi (1996) Identification of a novel protein phosphatase 2A regulatory subunit highly expressed in muscle. J. Biol. Chem. 271:5164-5170.
59. Trojanowski, J.Q. and V.M. Lee (1994) Phosphorylation of neuronal cytoskeletal proteins in Alzheimer's disease and Lewy body dementias. Ann. N.Y. Acad. Sci. 747:92-109.
60. Wadzinski, B.E., W.H. Wheat, S. Jaspers, L.F. Peruski, Jr., R.L. Lickteig, G.L. Johnson, and D.J. Klemm (1993) Nuclear protein phosphatase 2A dephosphorylates protein kinase A-phosphorylated CREB and regulates CREB transcriptional stimulation. Mol. Cell. Biol. 13:2822-2834.
61. Wang, Y. and D.J. Burke (1997) Cdc55p, the B-type regulatory subunit of protein phosphatase 2A, has multiple functions in mitosis and is required for the kinetochore/spindle checkpoint in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:620-626.
62. Wera, S. and B.A. Hemmings (1995) Serine/threonine protein phosphata-ses. Biochem. J. 311:17-29.
63. Zaucha, J.A., R.S. Westphal, and B.E. Wadzinski (1998) Protein phosphatase 2A regulatory subunits: cDNA cloning and analysis of mRNA expression. In J.W. Ludlow (ed): Protein Serine/Threonine Phosphatases. Clifton, NJ: Humana Press (in press).
64. Zhao, Y, G. Boguslawski, R.S. Zitomer, and A.A. DePaoli-Roach (1997) Sacharomyces cerevisiae homologues of mammalian B and B′ subunits of protein phosphatase 2A direct the enzyme to distinct cellular functions. J. Biol. Chem. 272:8256-8262.
65. Zolnierowicz, S., C. Csortos, J. Bondor, A. Verin, M.C. Mumby, and A.A. DePaoli-Roach (1994) Diversity in the regulatory B-subunits of protein phosphatase 2A: Identification of a novel isoform highly expressed in brain. Biochemistry 33:11858-11867.
66. Zolnierowicz, S., C. Van Hoof, N. Andjelkovic, P. Cron, I. Stevens, W Merlevede, J. Goris, and B.A. Hemmings (1996) The variable subunit associated with protein phosphatase 2A0 defines a novel multimember family of regulatory subunits. Biochem. J. 317:187-194.