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PMID: 1849074 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A role for the p34cdc2 kinase and phosphatases in the regulation of phosphorylation and disassembly of lamin B2 during the cell cycle.

The EMBO journal ·Vol. 10 ·No. 4 ·1991-04-00 ·Pages 865-75

Lüscher B, Brizuela L, Beach D, Eisenman RN

Abstract

While the p34cdc2 kinase is considered to be a critical regulator of mitosis, its function has not yet been directly linked to one of the key events during the onset of mitosis: nuclear envelope breakdown. Here we show that a major structural protein of the nuclear envelope, lamin B2, is phosphorylated by p34cdc2. Results from two-dimensional phosphopeptide mapping experiments demonstrate that the p34cdc2-specific phosphopeptides represent both mitotic and interphase specific phosphorylations of lamin B2 and include the major interphase phosphorylation site. In mitotic cells we detected two distinct forms of lamin B2 which differ in electrophoretic mobility and in degree of phosphorylation. The phosphorylation pattern of lamin B2 generated in vitro by p34cdc2 was more closely related to the less phosphorylated mitotic lamin B2, suggesting that another kinase(s) in addition to p34cdc2 is involved in generating the mitotic phosphorylation pattern. In addition, we show that treatment of interphase cells with okadaic acid, a potent phosphatase inhibitor, leads to the acquisition of mitosis-specific phosphopeptides and can reversibly increase the detergent-solubility of lamin B2. However, the M-phase-like phosphorylation of lamin B2 in itself is not sufficient to induce its disassembly from the nuclear lamina suggesting that an additional event(s) besides phosphorylation is required.

MeSH Terms
Animals CDC2 Protein Kinase/metabolism Cell Cycle/drug effects Cell Line Ethers, Cyclic/pharmacology Lamin Type B Lamins Nuclear Envelope/ultrastructure Nuclear Proteins/metabolism Okadaic Acid Peptide Mapping Phosphopeptides/isolation & purification Phosphoric Monoester Hydrolases/metabolism Phosphorylation
Chemicals
Ethers, Cyclic Lamin Type B Lamins Nuclear Proteins Phosphopeptides lamin B2 Okadaic Acid CDC2 Protein Kinase Phosphoric Monoester Hydrolases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Lüscher B
Fred Hutchinson Cancer Research Center, Division of Basic Sciences, Seattle, WA 98104.
Brizuela L
Beach D
Eisenman R N
References (61)
61 references, click to expand
  1. Universal control mechanism regulating onset of M-phase.
    Nature. 1990 Apr 5;344(6266):503-8 PMID: 2138713
  2. Differential phosphorylation of c-Abl in cell cycle determined by cdc2 kinase and phosphatase activity.
    Science. 1990 Apr 13;248(4952):217-20 PMID: 2183353
  3. The nuclear envelope lamina is reversibly depolymerized during mitosis.
    Cell. 1980 Jan;19(1):277-87 PMID: 7357605
  4. Autoimmune response directed against conserved determinants of nuclear envelope proteins in a patient with linear scleroderma.
    Proc Natl Acad Sci U S A. 1983 Jul;80(14):4374-8 PMID: 6192431
  5. Production of large numbers of mitotic mammalian cells by use of the reversible microtubule inhibitor nocodazole. Nocodazole accumulated mitotic cells.
    Exp Cell Res. 1980 Apr;126(2):397-405 PMID: 6153987
  6. Immunocytochemical localization of the major polypeptides of the nuclear pore complex-lamina fraction. Interphase and mitotic distribution.
    J Cell Biol. 1978 Nov;79(2 Pt 1):546-66 PMID: 102651
  7. Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail.
    Cell. 1977 May;11(1):95-103 PMID: 194709
  8. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  9. Establishment of tumor cell lines cultured from chickens with avian lymphoid leukosis.
    Natl Inst Anim Health Q (Tokyo). 1974 Winter;14(4):163-73 PMID: 4375792
  10. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  11. Activation at M-phase of a protein kinase encoded by a starfish homologue of the cell cycle control gene cdc2+.
    Nature. 1988 Sep 15;335(6187):251-4 PMID: 3412486
  12. Mutations in the nuclear lamin proteins resulting in their aberrant assembly in the cytoplasm.
    EMBO J. 1988 Aug;7(8):2301-9 PMID: 3056713
  13. Functional organization of the nuclear envelope.
    Annu Rev Cell Biol. 1988;4:335-74 PMID: 2461721
  14. The fates of chicken nuclear lamin proteins during mitosis: evidence for a reversible redistribution of lamin B2 between inner nuclear membrane and elements of the endoplasmic reticulum.
    J Cell Biol. 1988 Aug;107(2):397-406 PMID: 3417755
  15. Nuclear function and organization: the potential of immunochemical approaches.
    Int Rev Cytol. 1988;110:27-92 PMID: 3053500
  16. Disassembly of the nucleus in mitotic extracts: membrane vesicularization, lamin disassembly, and chromosome condensation are independent processes.
    Cell. 1987 Jan 30;48(2):219-30 PMID: 3026636
  17. The nucleus: structure, function, and dynamics.
    Annu Rev Biochem. 1987;56:535-65 PMID: 3304144
  18. A cell free system to study reassembly of the nuclear envelope at the end of mitosis.
    Cell. 1986 Feb 28;44(4):639-52 PMID: 3948244
  19. A human T lymphoblastic cell line lacks lamins A and C.
    EMBO J. 1987 Dec 1;6(12):3795-9 PMID: 3501373
  20. The nuclear lamin protein family in higher vertebrates. Identification of quantitatively minor lamin proteins by monoclonal antibodies.
    J Biol Chem. 1986 Oct 5;261(28):13293-301 PMID: 3531199
  21. Fission yeast p13 blocks mitotic activation and tyrosine dephosphorylation of the Xenopus cdc2 protein kinase.
    Cell. 1989 Jul 14;58(1):181-91 PMID: 2473838
  22. The fission yeast cdc2/cdc13/suc1 protein kinase: regulation of catalytic activity and nuclear localization.
    Cell. 1989 Aug 11;58(3):485-97 PMID: 2569363
  23. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis.
    Nature. 1989 Nov 2;342(6245):39-45 PMID: 2682257
  24. Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2+.
    Cell. 1988 Jul 29;54(3):433-9 PMID: 3293803
  25. Involvement of protein phosphatases 1 and 2A in the control of M phase-promoting factor activity in starfish.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3347-54 PMID: 2574724
  26. Protein phosphatases come of age.
    J Biol Chem. 1989 Dec 25;264(36):21435-8 PMID: 2557326
  27. Nuclear lamins and cytoplasmic intermediate filament proteins: a growing multigene family.
    Cell. 1987 Jan 16;48(1):3-4 PMID: 3791413
  28. The nuclear lamins. A multigene family of proteins in evolution and differentiation.
    Exp Cell Res. 1986 Jan;162(1):1-10 PMID: 2415378
  29. Effects of the tumour promoter okadaic acid on intracellular protein phosphorylation and metabolism.
    Nature. 1989 Jan 5;337(6202):78-81 PMID: 2562908
  30. Drosophila nuclear lamin precursor Dm0 is translated from either of two developmentally regulated mRNA species apparently encoded by a single gene.
    J Cell Biol. 1988 Mar;106(3):585-96 PMID: 3126192
  31. Reversible tyrosine phosphorylation of cdc2: dephosphorylation accompanies activation during entry into mitosis.
    Cell. 1989 Jul 14;58(1):193-203 PMID: 2473839
  32. A second higher vertebrate B-type lamin. cDNA sequence determination and in vitro processing of chicken lamin B2.
    J Mol Biol. 1989 Aug 5;208(3):405-15 PMID: 2477550
  33. Mitosis-specific phosphorylation of p60c-src by p34cdc2-associated protein kinase.
    Cell. 1989 Jun 2;57(5):775-86 PMID: 2470513
  34. Purified maturation promoting factor phosphorylates pp60c-src at the sites phosphorylated during fibroblast mitosis.
    Cell. 1989 Jun 2;57(5):763-74 PMID: 2470512
  35. Altered phosphorylation and activation of pp60c-src during fibroblast mitosis.
    Cell. 1988 Mar 25;52(6):801-10 PMID: 2450676
  36. Protein kinase C mediates platelet-derived growth factor-induced tyrosine phosphorylation of p42.
    J Cell Biol. 1988 Apr;106(4):1395-402 PMID: 2452172
  37. A 60 kd cdc2-associated polypeptide complexes with the E1A proteins in adenovirus-infected cells.
    Cell. 1989 Sep 8;58(5):981-90 PMID: 2570639
  38. Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2.
    Cell. 1989 Sep 8;58(5):833-46 PMID: 2570636
  39. Phosphorylation of large tumour antigen by cdc2 stimulates SV40 DNA replication.
    Nature. 1989 Oct 12;341(6242):503-7 PMID: 2552322
  40. Mammalian growth-associated H1 histone kinase: a homolog of cdc2+/CDC28 protein kinases controlling mitotic entry in yeast and frog cells.
    Mol Cell Biol. 1989 Sep;9(9):3860-8 PMID: 2550805
  41. Dephosphorylation and activation of Xenopus p34cdc2 protein kinase during the cell cycle.
    Nature. 1989 Jun 22;339(6226):626-9 PMID: 2543932
  42. Cdc2 protein kinase is complexed with both cyclin A and B: evidence for proteolytic inactivation of MPF.
    Cell. 1989 Mar 10;56(5):829-38 PMID: 2538242
  43. Activation of human CDC2 protein as a histone H1 kinase is associated with complex formation with the p62 subunit.
    Proc Natl Acad Sci U S A. 1989 Jun;86(12):4362-6 PMID: 2543971
  44. Phosphorylation of RNA polymerase by the murine homologue of the cell-cycle control protein cdc2.
    Nature. 1989 Jun 29;339(6227):679-84 PMID: 2662013
  45. Myc oncoproteins are phosphorylated by casein kinase II.
    EMBO J. 1989 Apr;8(4):1111-9 PMID: 2663470
  46. Purification of MPF from starfish: identification as the H1 histone kinase p34cdc2 and a possible mechanism for its periodic activation.
    Cell. 1989 Apr 21;57(2):253-63 PMID: 2649251
  47. Cloning and sequencing of cDNA clones encoding chicken lamins A and B1 and comparison of the primary structures of vertebrate A- and B-type lamins.
    J Mol Biol. 1989 Aug 5;208(3):393-404 PMID: 2795656
  48. Purification of maturation-promoting factor, an intracellular regulator of early mitotic events.
    Proc Natl Acad Sci U S A. 1988 May;85(9):3009-13 PMID: 3283736
  49. Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B.
    Cell. 1987 Nov 6;51(3):383-92 PMID: 3311384
  50. Differential expression of nuclear lamin proteins during chicken development.
    J Cell Biol. 1987 Jul;105(1):577-87 PMID: 3301871
  51. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins.
    Nature. 1986 Feb 6-12;319(6053):463-8 PMID: 3453101
  52. A fractionated cell-free system for analysis of prophase nuclear disassembly.
    J Cell Biol. 1986 Dec;103(6 Pt 1):2073-81 PMID: 3782291
  53. The nuclear lamina is a meshwork of intermediate-type filaments.
    Nature. 1986 Oct 9-15;323(6088):560-4 PMID: 3762708
  54. V-myc- and c-myc-encoded proteins are associated with the nuclear matrix.
    Mol Cell Biol. 1985 Jan;5(1):114-26 PMID: 3872410
  55. Phosphorylation of the nuclear lamins during interphase and mitosis.
    J Biol Chem. 1985 Jan 10;260(1):624-32 PMID: 3965465
  56. In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase.
    Cell. 1990 May 18;61(4):591-602 PMID: 2188731
  57. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis.
    Cell. 1990 May 18;61(4):579-89 PMID: 2344612
  58. Identification of cell cycle-regulated phosphorylation sites on nuclear lamin C.
    Cell. 1990 May 18;61(4):561-77 PMID: 2188730
  59. Okadaic acid mimics the action of insulin in stimulating protein kinase activity in isolated adipocytes. The role of protein phosphatase 2a in attenuation of the signal.
    J Biol Chem. 1990 Sep 25;265(27):16571-80 PMID: 2168895
  60. Okadaic acid: a new probe for the study of cellular regulation.
    Trends Biochem Sci. 1990 Mar;15(3):98-102 PMID: 2158158
  61. Identification of major nucleolar proteins as candidate mitotic substrates of cdc2 kinase.
    Cell. 1990 Mar 9;60(5):791-801 PMID: 2178776
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1991-04-00
Pages
865-75
Language
English
Region
England
NLM ID
8208664
PMCID
PMC452727
Subset
IM
Grants
NIGMS NIH HHS · GM39620 · United States
NCI NIH HHS · P01 CA 28151 · United States
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