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W2032936612 abstract "Disassembly of the sperm nuclear envelope at fertilization is one of the earliest events in the development of the male pronucleus. We report that nuclear lamina disassembly in interphase sea urchin egg cytosol is a result of lamin B phosphorylation mediated by protein kinase C (PKC). Lamin B of permeabilized sea urchin sperm nuclei incubated in fertilized egg G1 phase cytosolic extract is phosphorylated within 1 min of incubation and solubilized prior to sperm chromatin decondensation. Phosphorylation is Ca2+-dependent. It is reversibly inhibited by the PKC-specific inhibitor chelerythrine, a PKC pseudosubstrate inhibitor peptide, and a PKC substrate peptide, but not by inhibitors of PKA, p34 cdc2 or calmodulin kinase II. Phosphorylation is inhibited by immunodepletion of cytosolic PKC and restored by addition of purified rat brain PKC. Sperm lamin B is a substrate for rat brain PKC in vitro, resulting in lamin B solubilization. Two-dimensional phosphopeptide maps of lamin B phosphorylated by the cytosolic kinase and by purified rat PKC are virtually identical. These data suggest that PKC is the major kinase required for interphase disassembly of the sperm lamina. Disassembly of the sperm nuclear envelope at fertilization is one of the earliest events in the development of the male pronucleus. We report that nuclear lamina disassembly in interphase sea urchin egg cytosol is a result of lamin B phosphorylation mediated by protein kinase C (PKC). Lamin B of permeabilized sea urchin sperm nuclei incubated in fertilized egg G1 phase cytosolic extract is phosphorylated within 1 min of incubation and solubilized prior to sperm chromatin decondensation. Phosphorylation is Ca2+-dependent. It is reversibly inhibited by the PKC-specific inhibitor chelerythrine, a PKC pseudosubstrate inhibitor peptide, and a PKC substrate peptide, but not by inhibitors of PKA, p34 cdc2 or calmodulin kinase II. Phosphorylation is inhibited by immunodepletion of cytosolic PKC and restored by addition of purified rat brain PKC. Sperm lamin B is a substrate for rat brain PKC in vitro, resulting in lamin B solubilization. Two-dimensional phosphopeptide maps of lamin B phosphorylated by the cytosolic kinase and by purified rat PKC are virtually identical. These data suggest that PKC is the major kinase required for interphase disassembly of the sperm lamina. The nuclear lamina consists of a polymeric network of intermediate filament molecules, the nuclear lamins, underlying the inner nuclear membrane. The lamina is a dynamic structure, undergoing expansion during interphase of the cell cycle, and depolymerization at mitosis upon breakdown of the nuclear envelope (NE) 1The abbreviations used are: NE, nuclear envelope; BAPTA, 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid; DMAP, 6-dimethylaminopurine; NB, nuclear buffer; PAGE, polyacrylamide gel electrophoresis; PKA, protein kinase A (cAMP-dependent protein kinase); PKC, protein kinase C (Ca2+-dependent protein kinase); PKI, PKA inhibitor; CaM, calmodulin.1The abbreviations used are: NE, nuclear envelope; BAPTA, 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid; DMAP, 6-dimethylaminopurine; NB, nuclear buffer; PAGE, polyacrylamide gel electrophoresis; PKA, protein kinase A (cAMP-dependent protein kinase); PKC, protein kinase C (Ca2+-dependent protein kinase); PKI, PKA inhibitor; CaM, calmodulin. (1Gerace L. Blobel G. Cell. 1980; 19: 277-287Abstract Full Text PDF PubMed Scopus (594) Google Scholar). Mitotic disassembly and reassembly of the lamina is regulated by reversible lamin phosphorylation and dephosphorylation (1Gerace L. Blobel G. Cell. 1980; 19: 277-287Abstract Full Text PDF PubMed Scopus (594) Google Scholar). Interphase lamin phosphorylation has also been reported (2Ottaviano Y. Gerace L. J. Biol. Chem. 1985; 260: 624-632Abstract Full Text PDF PubMed Google Scholar, 3Smith D.E. Gruenbaum Y. Berrios M. Fisher P.A. J. Cell Biol. 1987; 105: 771-790Crossref PubMed Scopus (68) Google Scholar, 4Hornbeck P. Huang K.P. Paul W.E. Proc. Natl. Acad. Sci. U. S. A. 1988; 85: 2279-2283Crossref PubMed Scopus (69) Google Scholar, 5Stuurman N. Maus N. Fisher P.A. J. Cell Sci. 1995; 108: 3137-3144PubMed Google Scholar, 6Kill I.R. Hutchison C.J. FEBS Lett. 1995; 377: 26-30Crossref PubMed Scopus (22) Google Scholar), but its significance is not fully understood.Several lamin kinases have been identified that promote mitotic lamina solubilization or inhibit lamina assembly in vitro. They include cyclin B/p34 cdc2 (7Peter M. Nakagawa J. Dorée M. Labbé J.-C. Nigg E.A. Cell. 1990; 61: 591-602Abstract Full Text PDF PubMed Scopus (548) Google Scholar), S6 kinase II (8Ward G.E. Kirschner M.W. Cell. 1990; 61: 561-577Abstract Full Text PDF PubMed Scopus (273) Google Scholar), protein kinase C (PKC) (4Hornbeck P. Huang K.P. Paul W.E. Proc. Natl. Acad. Sci. U. S. A. 1988; 85: 2279-2283Crossref PubMed Scopus (69) Google Scholar, 9Fields A.P. Petit G.R. May W.S. J. Biol. Chem. 1988; 263: 8253-8260Abstract Full Text PDF PubMed Google Scholar), and the cAMP-dependent protein kinase PKA (10Stuurman N. FEBS Lett. 1997; 401: 171-174Crossref PubMed Scopus (27) Google Scholar). Down-regulation of PKA has also been shown to be essential for mitotic lamina disassembly (11Lamb N.J.C. Cavadore J.-C. Labbé J.-C. Mauer R.A. Fernandez A. EMBO J. 1991; 10: 1523-1533Crossref PubMed Scopus (74) Google Scholar). Although not a lamin kinase, Ca2+/calmodulin-dependent kinase II (CaM kinase II) is also involved in mitotic NE breakdown in sea urchin embryos (12Baitinger C. Alderton J. Poenie M. Schulman H. Steinhardt R.A. J. Cell Biol. 1990; 111: 1763-1773Crossref PubMed Scopus (139) Google Scholar). PKC has also been shown to phosphorylate chicken lamin B2 in interphase, a process thought to regulate lamin import into the nucleus (13Hennekes H. Peter M. Nigg E.A. J. Cell Biol. 1993; 120: 1293-1304Crossref PubMed Scopus (102) Google Scholar). These observations imply that multiple kinases regulate the dynamics of the nuclear lamina during the cell cycle.The transformation of the sea urchin sperm nucleus into a pronucleus at fertilization provides an opportunity to investigate NE assembly/disassembly during interphase. Sea urchin eggs are fertilized in G1 phase of the first cell cycle after completion of both meiotic divisions. At fertilization, the sperm NE vesiculates and a new NE reforms around the male pronucleus as the sperm chromatin decondenses (14Longo F.J. Anderson E. J. Cell Biol. 1968; 39: 335-368Crossref Scopus (191) Google Scholar). Male pronuclear formation has been duplicated in a cell-free system by incubating detergent-permeabilized sperm nuclei in fertilized egg extracts (15Cameron L.A. Poccia D.L. Dev. Biol. 1994; 162: 568-578Crossref PubMed Scopus (60) Google Scholar, 16Collas P. Poccia D.L. Dev. Biol. 1995; 169: 123-135Crossref PubMed Scopus (41) Google Scholar, 17Collas P. Poccia D.L. J. Cell Sci. 1996; 109: 1275-1283Crossref PubMed Google Scholar, 18Collas P. Pinto-Correia C. Poccia D.L. Exp. Cell Res. 1995; 219: 687-698Crossref PubMed Scopus (23) Google Scholar, 19Collas P. Courvalin J.-C. Poccia D.L. J. Cell Biol. 1996; 135: 1715-1725Crossref PubMed Scopus (94) Google Scholar). Detergent-permeabilized sperm nuclei retain their lamina, which consists of a major 65-kDa B-type lamin (referred to as lamin B) and several minor uncharacterized lamin epitope-containing peptides (18Collas P. Pinto-Correia C. Poccia D.L. Exp. Cell Res. 1995; 219: 687-698Crossref PubMed Scopus (23) Google Scholar). The first step of male pronucleus formation in vitro is the disassembly of the sperm nuclear lamina. The pronuclear lamina is reassembled only following formation of the nuclear membranes during nuclear swelling (19Collas P. Courvalin J.-C. Poccia D.L. J. Cell Biol. 1996; 135: 1715-1725Crossref PubMed Scopus (94) Google Scholar).Interphase lamina disassembly requires ATP hydrolysis, consistent with the involvement of protein kinase(s) (18Collas P. Pinto-Correia C. Poccia D.L. Exp. Cell Res. 1995; 219: 687-698Crossref PubMed Scopus (23) Google Scholar). One kinase activated at fertilization in the sea urchin is PKC. Fertilization stimulates phospholipase C in the egg plasma membrane, releasing diacylglycerol and inositol 1,4,5-trisphosphate from phosphoinositides. Increased inositol 1,4,5-trisphosphate triggers an intracellular release of Ca2+, which together with diacylglycerol activates PKC (20Nishizuka Y. Science. 1986; 233: 305-312Crossref PubMed Scopus (4018) Google Scholar). Activated soluble PKC has been shown to translocate to the plasma membrane (21Olds J.L. Favit A. Nelson T. Ascoli G. Gerstein A. Cameron M. Cameron L. Lesterm D. Rakow T. De Barry J. Toshioka T. Freyberg Z. Baru J. Alkon D.L. Dev. Biol. 1995; 172: 675-682Crossref PubMed Scopus (24) Google Scholar). Translocation of activated PKC to non-plasma membranes, such as the NE, has also been reported, as PKC moves to the nucleus of cultured mammalian cells upon mitogenic stimulation (9Fields A.P. Petit G.R. May W.S. J. Biol. Chem. 1988; 263: 8253-8260Abstract Full Text PDF PubMed Google Scholar, 22Fields A.P. Pincus S.M. Kraft A.S. May W.S. J. Biol. Chem. 1989; 264: 21896-21901Abstract Full Text PDF PubMed Google Scholar, 23Hocevar B.A. Fields A.P. J. Biol. Chem. 1991; 266: 28-33Abstract Full Text PDF PubMed Google Scholar). A sea urchin PKC isoform (suPKC1) has been cloned (24Rakow T.L. Shen S.S. Dev. Growth Differ. 1994; 36: 489-497Crossref Scopus (10) Google Scholar) and several substrates proposed (21Olds J.L. Favit A. Nelson T. Ascoli G. Gerstein A. Cameron M. Cameron L. Lesterm D. Rakow T. De Barry J. Toshioka T. Freyberg Z. Baru J. Alkon D.L. Dev. Biol. 1995; 172: 675-682Crossref PubMed Scopus (24) Google Scholar, 25Shen S.S. Buck W.R. Dev. Biol. 1990; 140: 272-280Crossref PubMed Scopus (48) Google Scholar). However, no lamin kinase activity has been attributed to fertilization-activated PKC.We report here that phosphorylation of sperm nuclear lamin B precedes its solubilization, in an interphase egg cytosolic extract, and provide evidence that this phosphorylation is mediated by PKC. Lamin B phosphorylation and solubilization precedes decondensation of the sperm chromatin, but is not sufficient to promote chromatin decondensation. The nuclear lamina consists of a polymeric network of intermediate filament molecules, the nuclear lamins, underlying the inner nuclear membrane. The lamina is a dynamic structure, undergoing expansion during interphase of the cell cycle, and depolymerization at mitosis upon breakdown of the nuclear envelope (NE) 1The abbreviations used are: NE, nuclear envelope; BAPTA, 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid; DMAP, 6-dimethylaminopurine; NB, nuclear buffer; PAGE, polyacrylamide gel electrophoresis; PKA, protein kinase A (cAMP-dependent protein kinase); PKC, protein kinase C (Ca2+-dependent protein kinase); PKI, PKA inhibitor; CaM, calmodulin.1The abbreviations used are: NE, nuclear envelope; BAPTA, 1,2-bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid; DMAP, 6-dimethylaminopurine; NB, nuclear buffer; PAGE, polyacrylamide gel electrophoresis; PKA, protein kinase A (cAMP-dependent protein kinase); PKC, protein kinase C (Ca2+-dependent protein kinase); PKI, PKA inhibitor; CaM, calmodulin. (1Gerace L. Blobel G. Cell. 1980; 19: 277-287Abstract Full Text PDF PubMed Scopus (594) Google Scholar). Mitotic disassembly and reassembly of the lamina is regulated by reversible lamin phosphorylation and dephosphorylation (1Gerace L. Blobel G. Cell. 1980; 19: 277-287Abstract Full Text PDF PubMed Scopus (594) Google Scholar). Interphase lamin phosphorylation has also been reported (2Ottaviano Y. Gerace L. J. Biol. Chem. 1985; 260: 624-632Abstract Full Text PDF PubMed Google Scholar, 3Smith D.E. Gruenbaum Y. Berrios M. Fisher P.A. J. Cell Biol. 1987; 105: 771-790Crossref PubMed Scopus (68) Google Scholar, 4Hornbeck P. Huang K.P. Paul W.E. Proc. Natl. Acad. Sci. U. S. A. 1988; 85: 2279-2283Crossref PubMed Scopus (69) Google Scholar, 5Stuurman N. Maus N. Fisher P.A. J. Cell Sci. 1995; 108: 3137-3144PubMed Google Scholar, 6Kill I.R. Hutchison C.J. FEBS Lett. 1995; 377: 26-30Crossref PubMed Scopus (22) Google Scholar), but its significance is not fully understood. Several lamin kinases have been identified that promote mitotic lamina solubilization or inhibit lamina assembly in vitro. They include cyclin B/p34 cdc2 (7Peter M. Nakagawa J. Dorée M. Labbé J.-C. Nigg E.A. Cell. 1990; 61: 591-602Abstract Full Text PDF PubMed Scopus (548) Google Scholar), S6 kinase II (8Ward G.E. Kirschner M.W. Cell. 1990; 61: 561-577Abstract Full Text PDF PubMed Scopus (273) Google Scholar), protein kinase C (PKC) (4Hornbeck P. Huang K.P. Paul W.E. Proc. Natl. Acad. Sci. U. S. A. 1988; 85: 2279-2283Crossref PubMed Scopus (69) Google Scholar, 9Fields A.P. Petit G.R. May W.S. J. Biol. Chem. 1988; 263: 8253-8260Abstract Full Text PDF PubMed Google Scholar), and the cAMP-dependent protein kinase PKA (10Stuurman N. FEBS Lett. 1997; 401: 171-174Crossref PubMed Scopus (27) Google Scholar). Down-regulation of PKA has also been shown to be essential for mitotic lamina disassembly (11Lamb N.J.C. Cavadore J.-C. Labbé J.-C. Mauer R.A. Fernandez A. EMBO J. 1991; 10: 1523-1533Crossref PubMed Scopus (74) Google Scholar). Although not a lamin kinase, Ca2+/calmodulin-dependent kinase II (CaM kinase II) is also involved in mitotic NE breakdown in sea urchin embryos (12Baitinger C. Alderton J. Poenie M. Schulman H. Steinhardt R.A. J. Cell Biol. 1990; 111: 1763-1773Crossref PubMed Scopus (139) Google Scholar). PKC has also been shown to phosphorylate chicken lamin B2 in interphase, a process thought to regulate lamin import into the nucleus (13Hennekes H. Peter M. Nigg E.A. J. Cell Biol. 1993; 120: 1293-1304Crossref PubMed Scopus (102) Google Scholar). These observations imply that multiple kinases regulate the dynamics of the nuclear lamina during the cell cycle. The transformation of the sea urchin sperm nucleus into a pronucleus at fertilization provides an opportunity to investigate NE assembly/disassembly during interphase. Sea urchin eggs are fertilized in G1 phase of the first cell cycle after completion of both meiotic divisions. At fertilization, the sperm NE vesiculates and a new NE reforms around the male pronucleus as the sperm chromatin decondenses (14Longo F.J. Anderson E. J. Cell Biol. 1968; 39: 335-368Crossref Scopus (191) Google Scholar). Male pronuclear formation has been duplicated in a cell-free system by incubating detergent-permeabilized sperm nuclei in fertilized egg extracts (15Cameron L.A. Poccia D.L. Dev. Biol. 1994; 162: 568-578Crossref PubMed Scopus (60) Google Scholar, 16Collas P. Poccia D.L. Dev. Biol. 1995; 169: 123-135Crossref PubMed Scopus (41) Google Scholar, 17Collas P. Poccia D.L. J. Cell Sci. 1996; 109: 1275-1283Crossref PubMed Google Scholar, 18Collas P. Pinto-Correia C. Poccia D.L. Exp. Cell Res. 1995; 219: 687-698Crossref PubMed Scopus (23) Google Scholar, 19Collas P. Courvalin J.-C. Poccia D.L. J. Cell Biol. 1996; 135: 1715-1725Crossref PubMed Scopus (94) Google Scholar). Detergent-permeabilized sperm nuclei retain their lamina, which consists of a major 65-kDa B-type lamin (referred to as lamin B) and several minor uncharacterized lamin epitope-containing peptides (18Collas P. Pinto-Correia C. Poccia D.L. Exp. Cell Res. 1995; 219: 687-698Crossref PubMed Scopus (23) Google Scholar). The first step of male pronucleus formation in vitro is the disassembly of the sperm nuclear lamina. The pronuclear lamina is reassembled only following formation of the nuclear membranes during nuclear swelling (19Collas P. Courvalin J.-C. Poccia D.L. J. Cell Biol. 1996; 135: 1715-1725Crossref PubMed Scopus (94) Google Scholar). Interphase lamina disassembly requires ATP hydrolysis, consistent with the involvement of protein kinase(s) (18Collas P. Pinto-Correia C. Poccia D.L. Exp. Cell Res. 1995; 219: 687-698Crossref PubMed Scopus (23) Google Scholar). One kinase activated at fertilization in the sea urchin is PKC. Fertilization stimulates phospholipase C in the egg plasma membrane, releasing diacylglycerol and inositol 1,4,5-trisphosphate from phosphoinositides. Increased inositol 1,4,5-trisphosphate triggers an intracellular release of Ca2+, which together with diacylglycerol activates PKC (20Nishizuka Y. Science. 1986; 233: 305-312Crossref PubMed Scopus (4018) Google Scholar). Activated soluble PKC has been shown to translocate to the plasma membrane (21Olds J.L. Favit A. Nelson T. Ascoli G. Gerstein A. Cameron M. Cameron L. Lesterm D. Rakow T. De Barry J. Toshioka T. Freyberg Z. Baru J. Alkon D.L. Dev. Biol. 1995; 172: 675-682Crossref PubMed Scopus (24) Google Scholar). Translocation of activated PKC to non-plasma membranes, such as the NE, has also been reported, as PKC moves to the nucleus of cultured mammalian cells upon mitogenic stimulation (9Fields A.P. Petit G.R. May W.S. J. Biol. Chem. 1988; 263: 8253-8260Abstract Full Text PDF PubMed Google Scholar, 22Fields A.P. Pincus S.M. Kraft A.S. May W.S. J. Biol. Chem. 1989; 264: 21896-21901Abstract Full Text PDF PubMed Google Scholar, 23Hocevar B.A. Fields A.P. J. Biol. Chem. 1991; 266: 28-33Abstract Full Text PDF PubMed Google Scholar). A sea urchin PKC isoform (suPKC1) has been cloned (24Rakow T.L. Shen S.S. Dev. Growth Differ. 1994; 36: 489-497Crossref Scopus (10) Google Scholar) and several substrates proposed (21Olds J.L. Favit A. Nelson T. Ascoli G. Gerstein A. Cameron M. Cameron L. Lesterm D. Rakow T. De Barry J. Toshioka T. Freyberg Z. Baru J. Alkon D.L. Dev. Biol. 1995; 172: 675-682Crossref PubMed Scopus (24) Google Scholar, 25Shen S.S. Buck W.R. Dev. Biol. 1990; 140: 272-280Crossref PubMed Scopus (48) Google Scholar). However, no lamin kinase activity has been attributed to fertilization-activated PKC. We report here that phosphorylation of sperm nuclear lamin B precedes its solubilization, in an interphase egg cytosolic extract, and provide evidence that this phosphorylation is mediated by PKC. Lamin B phosphorylation and solubilization precedes decondensation of the sperm chromatin, but is not sufficient to promote chromatin decondensation. We are grateful to Dr. Jon Holy (University of Minnesota, Duluth) for the gift of the W3-1 antibody, Dr. Laurent Meijer (CNRS, Roscoff, France) for the gift of olomoucine and roscovitine, Dr. Sheldon Shen (Iowa State University) for the gift of the anti-PKC antibody, and Dr. Howard Worman (Columbia University) for critical reading of the manuscript." @default.
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W2032936612 title "Protein Kinase C-mediated Interphase Lamin B Phosphorylation and Solubilization" @default.
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