Nucleomorphin

Probing of Dictyostelium discoideum cell extracts after SDS-PAGE using 35S-recombinant calmodulin (CaM) as a probe has revealed approximately three-dozen Ca2+-dependent calmodulin binding proteins. Here, we report the molecular cloning, expression, and subcellular localization of a gene encoding a novel calmodulin-binding protein (CaMBP); we have called nucleomorphin, from D. discoideum. A λZAP cDNA expression library of cells from multicellular development was screened using a recombinant calmodulin probe (35S-VU1-CaM). The open reading frame of 1119 nucleotides encodes a polypeptide of 340 amino acids with a calculated molecular mass of 38.7 kDa and is constitutively expressed throughout the Dictyostelium life cycle. Nucleomorphin contains a highly acidic glutamic/aspartic acid inverted repeat (DEED) with significant similarity to the conserved nucleoplasmin domain and a putative transmembrane domain in the carboxyl-terminal region. Southern blotting reveals that nucleomorphin exists as a single copy gene. Using gel overlay assays and CaM-agarose we show that bacterially expressed nucleomorphin binds to bovine CaM in a Ca2+-dependent manner. Amino-terminal fusion to the green fluorescence protein (GFP) showed that GFP-NumA localized to the nucleus as distinct arc-like patterns similar to heterochromatin regions. GFP-NumA lacking the acidic DEED repeat still showed arc-like accumulations at the nuclear periphery, but the number of nuclei in these cells was increased markedly compared with control cells. Cells expressing GFP-NumA lacking the transmembrane domain localized to the nuclear periphery but did not affect nuclear number or gross morphology. Nucleomorphin is the first nuclear CaMBP to be identified in Dictyostelium. Furthermore, these data present the first identification of a member of the nucleoplasmin family as a calmodulin-binding protein and suggest nucleomorphin has a role in nuclear structure in Dictyostelium. Probing of Dictyostelium discoideum cell extracts after SDS-PAGE using 35S-recombinant calmodulin (CaM) as a probe has revealed approximately three-dozen Ca2+-dependent calmodulin binding proteins. Here, we report the molecular cloning, expression, and subcellular localization of a gene encoding a novel calmodulin-binding protein (CaMBP); we have called nucleomorphin, from D. discoideum. A λZAP cDNA expression library of cells from multicellular development was screened using a recombinant calmodulin probe (35S-VU1-CaM). The open reading frame of 1119 nucleotides encodes a polypeptide of 340 amino acids with a calculated molecular mass of 38.7 kDa and is constitutively expressed throughout the Dictyostelium life cycle. Nucleomorphin contains a highly acidic glutamic/aspartic acid inverted repeat (DEED) with significant similarity to the conserved nucleoplasmin domain and a putative transmembrane domain in the carboxyl-terminal region. Southern blotting reveals that nucleomorphin exists as a single copy gene. Using gel overlay assays and CaM-agarose we show that bacterially expressed nucleomorphin binds to bovine CaM in a Ca2+-dependent manner. Amino-terminal fusion to the green fluorescence protein (GFP) showed that GFP-NumA localized to the nucleus as distinct arc-like patterns similar to heterochromatin regions. GFP-NumA lacking the acidic DEED repeat still showed arc-like accumulations at the nuclear periphery, but the number of nuclei in these cells was increased markedly compared with control cells. Cells expressing GFP-NumA lacking the transmembrane domain localized to the nuclear periphery but did not affect nuclear number or gross morphology. Nucleomorphin is the first nuclear CaMBP to be identified in Dictyostelium. Furthermore, these data present the first identification of a member of the nucleoplasmin family as a calmodulin-binding protein and suggest nucleomorphin has a role in nuclear structure in Dictyostelium. Calmodulin (CaM 1The abbreviations used are: CaMcalmodulinCaMBPscalmodulin-binding proteinsCaMKCaM kinaseCIAPcalf-intestinal alkaline phosphataseDIGdigoxigeninGFPgreen fluorescent proteinHRPhorseradish peroxidaseLPSlower pad solutionMBPmaltose binding proteinPVDFpolyvinylidene difluorideCNcalcineurinNLSnuclear localization sequenceDEEDglutamic/aspartic acid inverted repeatIPTGisopropyl-β-d-thiogalactopyranosideBSAbovine serum albumin ), the major, essential Ca2+-binding protein of all eukaryotes, is highly conserved such that the CaM of mammals and of eukaryotic microbes, such as Dictyostelium discoideum, differs in only a few amino acids leaving them functionally identical (1Marshak D.R. Clarke M. Roberts D.M. Watterson D.M. Biochemistry. 1984; 23 (0): 2891-2899Crossref PubMed Scopus (82) Google Scholar, 2Klee C. Cohen C.B. Klee C.B. Calmodulin O. Elsevier Science Publishing, Inc., New York1988: 35-56Google Scholar, 3Friedberg F. Prot. Seq. Data Anal. 1991; 3: 335-337Google Scholar, 4Manlan A. Klee C.B. Adv. Cyclic Nucleotide Res. 1984; 201: 227-238Google Scholar). CaM is a small acidic protein consisting of a flexible α-helical tether joining two globular domains each of which contain two Ca2+-binding sites (5Haeich J. Klee C.B. Demaille J.G. Biochemistry. 1981; 20: 3890-3897Crossref PubMed Scopus (266) Google Scholar, 6Keller C.H. Olwin B.B. Laporte D.C. Storm D.R. Biochemistry. 1981; 21: 156-162Crossref Scopus (76) Google Scholar). Upon Ca2+binding, CaM undergoes a large conformational change exposing two hydrophobic patches that allow for target-protein interaction (7James P. Vorherr T. Carafoli E. Trends Biochem. Sci. 1995; 20: 38-42Abstract Full Text PDF PubMed Scopus (347) Google Scholar). CaM binding to its targets does not operate through a conserved motif, because CaM binding regions on target proteins show little sequence homology. Many Ca2+-dependent CaMBPs have one or more CaM-binding domains characterized by a basic amphipathic helix commonly with positively charged residues interspersed among hydrophobic and aromatic residues (7James P. Vorherr T. Carafoli E. Trends Biochem. Sci. 1995; 20: 38-42Abstract Full Text PDF PubMed Scopus (347) Google Scholar). α-Helical wheel analysis typically shows a segregation of hydrophobic residues on one side and basic charged residues on the other (8O'Neil K.T. DeGrado W.F. Trends Biol. Sci. 1990; 15: 59-64Abstract Full Text PDF PubMed Scopus (714) Google Scholar). Ca2+-dependent CaMBPs can be grouped into two related motifs (1-8-14 and 1-5-10) based on conserved hydrophobic residues (9Ikura M. Clore G.M. Gronenborn A.M. Zhu G. Klee C.B. Bax A. Science. 1992; 256: 632-638Crossref PubMed Scopus (1179) Google Scholar, 10Persechini A. Kretsinger R.H. J. Biol. Chem. 1988; 263: 12175-12178Abstract Full Text PDF PubMed Google Scholar, 11Rhoads A.R. Friedberg F. FASEB J. 1997; 11: 331-340Crossref PubMed Scopus Google Scholar). the and using the CaM and A.R. Friedberg F. FASEB J. 1997; 11: 331-340Crossref PubMed Scopus Google Scholar, M. T. J. Biol. Chem. Full Text PDF PubMed Google Scholar, D. A.M. O. J. Biol. Chem. Full Text PDF Google Scholar, J. Biol. Chem. Full Text PDF PubMed Google Scholar). CaMBPs that not these motifs and T. F. T. Carafoli E. Biochemistry. PubMed Scopus Google J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). Many CaMBPs to the of CaM and CaM in a through motif, as has for and the and Trends Biol. 1995; Full Text PDF PubMed Scopus Google Scholar, J. Biol. PubMed Scopus Google Scholar, Biol. 1992; PubMed Scopus Google Scholar). target proteins the a of and is as the of CaMBPs has not for cell calmodulin calmodulin-binding proteins CaM alkaline green fluorescent protein pad binding protein nuclear localization sequence glutamic/aspartic acid inverted repeat bovine serum albumin Dictyostelium has used as a for the of the molecular of cell and in eukaryotic cells The of Dictyostelium discoideum. New Scholar). Dictyostelium is and contains one CaM and (1Marshak D.R. Clarke M. Roberts D.M. Watterson D.M. Biochemistry. 1984; 23 (0): 2891-2899Crossref PubMed Scopus (82) Google Scholar). of D. discoideum cell extracts after SDS-PAGE using a recombinant CaM probe reveals Ca2+-dependent CaMBPs a CaMBP PubMed Scopus Google Scholar, Res. PubMed Scopus Google Scholar, Scopus Google Scholar, Biochem. Res. 201: PubMed Scopus Google Scholar). CaM and CaMBPs have to and in D. discoideum PubMed Scopus Google Scholar, Res. PubMed Scopus Google Scholar, Scopus Google Scholar, Biochem. Res. 201: PubMed Scopus Google Scholar, Res. 1988; PubMed Scopus Google Scholar, 1995; Scholar). number and essential in a number of only a few CaMBPs have characterized in Dictyostelium. a in has to be in cell J. Biol. Chem. 1997; Full Text Full Text PDF PubMed Scopus Google Scholar, J. Biol. Chem. 1997; Full Text Full Text PDF PubMed Scopus Google Scholar). CaM targets Trends Biol. 1995; Full Text PDF PubMed Scopus Google Scholar). for a CaMBP that binds show in and F. F. C. M. J. Sci. Google Scholar). for Dictyostelium a to T. M. J. Biol. 1997; PubMed Scopus Google has characterized J. Biochem. PubMed Scopus Google Scholar, Res. 1997; PubMed Scopus Google Scholar, Adv. Res. Google Scholar). and A not or but affect cell the and of Dictyostelium still analysis F. J. PubMed Google Scholar, A. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). to as CaMBPs targets based to subcellular and as in CaM D. J. C. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). all of the CaMBPs have revealed and of and CaM has to a λZAP cDNA expression library of cells from multicellular development using a recombinant CaM probe to encoding putative was the first cDNA that we and A number the protein of have used to novel CaMBPs in calmodulin-binding and a calmodulin-binding protein F. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, T. J. 20: PubMed Google Scholar). we report on the of a cDNA encoding a nuclear protein of 340 amino acids with a molecular mass of 38.7 kDa that contains nuclear localization acid inverted repeat of and acid residues is of the conserved nucleoplasmin domain is a member of the nucleoplasmin of nuclear proteins. have gene Southern blotting and that a single gene exists in the of D. discoideum. assays using fusion proteins show nucleomorphin to be a Ca2+-dependent CaM target protein that contains at two CaM-binding Nucleomorphin and protein each expressed throughout GFP-NumA localized to regions the periphery of the GFP-NumA lacking the putative transmembrane domain and the DEED repeat still at the periphery of the of the acidic to in these data that nucleomorphin is a nuclear calmodulin-binding protein and is related to which be in nuclear structure in Dictyostelium. used and from New from or and mass from and molecular and and molecular from from was from The was from of and of the cDNA library as J. T. A Scholar). in with to the of recombinant CaM as a of of in was and in of from to in and was with E. and at of was and a at for in and the of the and at from the and in and for in with and at for with of recombinant to in with and The of is M. Biol. Google Scholar). The with for a of and to for to on the and to to as cDNA for putative calmodulin-binding proteins. of the and of cells was to the with the from from by of J. T. A and to analysis using and with at the compared with in the Data using J. Biol. 1990; PubMed Scopus Google Scholar). motifs and the molecular and from the amino acid using the M. 1992; PubMed Scopus Google and the of D. discoideum was used as the Cells in at with a of E. and at for with pad and the cells to of with by Cells at a of in the of in and in a the Southern Dictyostelium nuclear was by The cells in of and A of of was and on for by at for at and in of and and for at with of and with was to and the was with of The was in with A. was using and and was on a gel and to a J. T. A Scholar). nucleomorphin cDNA was used as a was from and cells for the of was on a gel and to by blotting J. T. A Scholar). Southern and and using the and to the to the nucleomorphin open reading frame for amino acids through and sites to the and using the and Using the from was in a for consisting of a at for at for and at for A single was to into which with the using and to using and into E. 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T. A Scholar). each with of recombinant of of protein at and two after the as E. D. A Scholar). cells from at the in with and and to for protein was using the protein of protein was using a and in in and with at a of at for with for the was with the blotting using to fusion proteins and using the for in acid by with in in by for for and a with probe and for is for the in the probe at with in the probe M. Biol. Google Scholar). to for each in probe and in acid with and to for calmodulin and as with T. A. Biochem. Res. 1995; PubMed Scopus Google Scholar). of recombinant in of CaM-binding was for at on a with of CaM-agarose in the was with throughout the The was after and the was with of binding protein was by the of of and interaction was by SDS-PAGE or Cells by as with E. Biol. Full Text Full Text PDF PubMed Scopus Google Scholar). Cells in in for a of and to of and by Cells with and in of and of was Cells on for and to Cells with two of and a of with Cells to of and to for The was and with The was for a of be by the of using into of and to as the of GFP-NumA in cells to a of in at a of and to Cells to to the for a of which as a of to allow cells to that is cells with and fluorescent using a with a and a the was with a with a and using a to a cells from each and the number of nuclei cell was have used a interaction to encoding putative Ca2+-dependent CaM-binding proteins from cells of D. discoideum. A λZAP cDNA expression library from cells through development was screened using recombinant to on to in which the was by a of not the putative Ca2+-dependent two that for nucleomorphin, all of which CaM in a Ca2+-dependent manner. analysis of each cDNA revealed identical patterns for from the of the two revealed that Nucleomorphin is by a cDNA of 1119 The sequence and the amino acid sequence of gene in The cDNA contains a at the and the sequence of the differs from a sequence of D. Biochem. Res. 1991; PubMed Scopus Google Scholar). The at The Dictyostelium has in and Dictyostelium as Res. PubMed Scopus Google Scholar, T. T. 1990; 11: PubMed Scopus Google Scholar). of the sequence a single open reading frame encoding a protein of 340 amino acids with a calculated molecular mass of 38.7 kDa and of shows the amino acid sequence of nucleomorphin and domains is the acids and A of and is commonly in Dictyostelium proteins but is of M. J. Biol. Chem. 1997; Full Text Full Text PDF PubMed Scopus Google Scholar). analysis of nucleomorphin did not significant to protein nucleomorphin highly acidic domain acids that is of acid and acid which we the DEED has inverted repeat of which the A and of domain significant to nucleoplasmin proteins from a of protein from J. Biol. Chem. 1997; Full Text Full Text PDF PubMed Scopus Google protein from G. M. J. A. M. M. J. Biol. 1997; PubMed Scopus Google and from G. Res. 1990; PubMed Scopus Google Scholar). of the conserved domain using shows the of on analysis with M. 1992; PubMed Scopus Google nucleomorphin contains a putative transmembrane of because does not contain a sequence and the exists in the Trends Biol. 3: Full Text PDF PubMed Scopus Google Scholar). of nuclear localization reveals the of regions. in the amino acid sequence exists a with two more at and and The is with that of the at in the amino acid sequence conserved residues nucleomorphin at residues and nucleomorphin undergoes at of the sites in protein molecular mass of 38.7 kDa on SDS-PAGE with molecular mass of one the that the highly acidic of nucleomorphin in through SDS-PAGE to its to has by fusion protein using protein J. Biol. PubMed Scopus Google Scholar). The for CaM nucleomorphin and in the amino of nucleomorphin is a CaM-binding domain of the the contains two more a is present and a putative domain that contains of the of nucleoplasmin domains in of nucleomorphin protein protein nucleoplasmin that identical in all in residues in of Ca2+-dependent calmodulin-binding in nucleomorphin with CaM-binding proteins. motifs on the to the after the The of conserved hydrophobic residues which to role in the interaction with The cDNA was into expression and at of nucleomorphin as a fusion protein for using was The fusion protein from cell not be by of SDS-PAGE and was only using serum or not that the acid of was the of nucleomorphin in E. we a number of fusion the DEED repeat and and that the DEED repeat and expression of the DEED repeat only be using serum or the not of lacking the DEED repeat was and for the of each fusion protein as the was only in the was used to the of the CaM-binding analysis with showed that at two regions of CaM binding The protein does not binding the nucleomorphin the CaM binding domains as domain shows a segregation of basic charged residues to one side of the helix and hydrophobic residues on the of CaM to or was to be because binding to CaM was in the of A using CaM-agarose the Ca2+-dependent of CaM binding to have of nucleomorphin to the for CaM putative CaM-binding domains of nucleomorphin by wheel and CaM-binding wheel of the putative CaM-binding in nucleomorphin shows the segregation of hydrophobic and positively charged The amino domain residues domains residues and binding calmodulin to and and and of and with and of at with in probe and was for the in the probe and CaM was through to CaM-agarose of The was as extracts from cells expressing with of by in and using with and protein protein from mass of the fusion proteins in is Nucleomorphin expression was by of from cells at A single of was and to be expressed constitutively throughout development the of the protein was at by and and nucleomorphin was using nucleomorphin in nucleomorphin with molecular mass of kDa in SDS-PAGE and is present throughout The protein the first and to through development essential role for nucleomorphin in the life of Dictyostelium. Southern analysis was using the cDNA probe after of with the and The in the of two as because a single for in the of the cDNA and only one was in the that a single gene encoding nucleomorphin in the of D. discoideum. The was used with from the cDNA to the open reading frame using as the A single was identical in to the cDNA the gene for nucleomorphin is by not and the of the cDNA encoding analysis of from D. discoideum was with or on a to and with and on the have used a to the localization of nucleomorphin in the contains a transmembrane domain that for we to to the of The of GFP-NumA fluorescence in all of was compared with cells with that the fluorescence is to the fusion on protein extracts using a A was with a molecular mass of kDa to the mass of the fusion protein not a of kDa was the which the of we that fluorescence from cell to a related to the used to expression of the fusion protein M. PubMed Scopus Google Scholar, M. A. M. C. G. G. Biol. 1997; Full Text Full Text PDF PubMed Scopus Google Scholar). GFP-NumA was the nucleus as distinct arc-like that to domains to the nuclear J. Biol. PubMed Scopus (76) Google Cells with a for regions of to the nuclear localization of the shows GFP-NumA is localized nuclei with Cells expressing lacking the putative transmembrane domain or the acidic DEED repeat localization to domains at the periphery of nuclei cells expressing the a in with as as nuclei in one cell cells and the other GFP-NumA cell typically one or two nuclei and be that is and into the does not the a of of in the of the The number of nuclei cell was for each Cells expressing compared with GFP-NumA and with of the cells or more of the to the of the nuclei in the of cells with of we of the nuclear and and of the DEED repeat in Dictyostelium. in cells expressing GFP-NumA of the to in cells. The nuclei of cells for each the of the eukaryotic protein in we screened a λZAP cDNA expression library CaM to encoding of its target proteins. to identified on in the of a cDNA encoding a novel CaM-binding Using we have that the protein which we have called nucleomorphin, by the cDNA binds to CaM in a Ca2+-dependent manner. the cDNA was identified through binding to CaM was in the of but not not in using of nucleomorphin to nucleomorphin to in a Ca2+-dependent using overlay The CaM binding on the gel overlay similar CaM binds each fusion with have to contain CaM binding in the amino and J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). we have for amino acid residues in that the of CaM-binding wheel conserved hydrophobic to and (8O'Neil K.T. DeGrado W.F. Trends Biol. Sci. 1990; 15: 59-64Abstract Full Text PDF PubMed Scopus (714) Google Scholar, 11Rhoads A.R. Friedberg F. FASEB J. 1997; 11: 331-340Crossref PubMed Scopus Google Scholar). have identified CaM-binding domains in nucleomorphin based these regions of sequence show of other calmodulin-binding in that positively charged and contain of hydrophobic residues with aromatic residues The calmodulin-binding of and all show these F. Prot. Seq. Data Anal. 1991; 3: 335-337Google Scholar, P. Vorherr T. Carafoli E. Trends Biochem. Sci. 1995; 20: 38-42Abstract Full Text PDF PubMed Scopus (347) Google Scholar). the amino of nucleomorphin is a CaM-binding domain of the that was A.R. Friedberg F. FASEB J. 1997; 11: 331-340Crossref PubMed Scopus Google Scholar). The of domain is the of amino acids two hydrophobic CaMBPs of contain conserved hydrophobic residues at the is still at the of these residues the binding of the of nucleomorphin, a is present A putative CaM-binding domain can be in nucleomorphin that contains of the motif, in which two hydrophobic residues by amino but not CaMBPs with domain have a conserved hydrophobic at amino acid A.R. Friedberg F. FASEB J. 1997; 11: 331-340Crossref PubMed Scopus Google Scholar). The Ca2+-dependent binding of nucleomorphin was using expressed protein on CaM-agarose used the lacking the DEED repeat but the CaM-binding that of acidic residues was the of nucleomorphin in E. by on the for each charged in of the and to in the of the repeat only be using serum or the not The of CaM used in the of the library and CaM binding of the of CaM in the cell that nucleomorphin a role in Dictyostelium. we to the for CaM Data to a of the sequence contains a putative conserved domain of the of proteins as nucleomorphin is a nuclear the amino acid sequence of one is with that of the at in the amino acid sequence which is with nucleoplasmin C. J. Roberts J. Biol. 1988; PubMed Scopus Google Scholar). The of the in nucleomorphin has to be but to these regions by to is the of sites for such as protein and protein C. sites and nuclear localization of nucleoplasmin and M. Biochemistry. PubMed Scopus Google Scholar, C. J. J. Sci. 11: PubMed Google Scholar). Nucleomorphin is a highly acidic protein in to the acid of acid of nucleomorphin with of the nucleoplasmin family reveals sequence and to the acidic of family have one or more acidic domains consisting of a of to more acid and acid residues analysis shows that these two residues can more of the amino acids in proteins of in nucleomorphin, of the such as J. Biol. Chem. 1997; Full Text Full Text PDF PubMed Scopus Google contain acidic nucleomorphin does not contain of the nucleoplasmin nucleoplasmin and nucleoplasmin such domains G.M. A. PubMed Scopus Google Scholar). The DEED repeat the molecular mass in from and the molecular mass of nucleomorphin is the mass calculated from SDS-PAGE The mass be to the acidic of the protein as was for J. Biol. Chem. 1997; Full Text Full Text PDF PubMed Scopus Google Scholar). can to the in the of nucleomorphin is still with the acidic of nucleomorphin, the of proteins called have to contain of acidic residues J. Biol. Chem. 1997; Full Text Full Text PDF PubMed Scopus Google Scholar). proteins a that in structure and a significant binding to the in Full Text PDF PubMed Scopus Google Scholar, A. 1991; Full Text PDF PubMed Scopus Google Scholar). that the acidic domain nucleomorphin to to or other positively charged proteins. has that nucleoplasmin in binding to the and and is to be essential in and the of to be C. J. Roberts J. Biol. 1988; PubMed Scopus Google Scholar, A. 1991; Full Text PDF PubMed Scopus Google Scholar, J. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, J. J. Scopus Google Scholar). nucleomorphin and protein throughout development at of GFP-NumA was by blotting using and was that the present in was Furthermore, for the of fluorescence throughout the nucleomorphin expression is as to a GFP-NumA was localized to patches at the periphery of the of GFP-NumA lacking the putative transmembrane domain localized to the nuclear The fluorescence was similar to the but the arc-like was we the that nucleomorphin to the nuclear nucleomorphin with the of interaction be to localized to the nuclear periphery in the of the lacking the DEED repeat to its role in Dictyostelium. Cells expressing a in the number of nuclei cell with a the localization of nucleomorphin was not that the DEED repeat to in nuclear structure or The gene is present in cells with each of the but not at a to for the of of with the the of nuclear The of the nuclei did not to be by of the used in the of cells with large of nuclei as was in one cell with cells to be in have these through the of nuclear and and be to the of the nuclei in the cells is to nucleomorphin by of have more of the to nucleomorphin in to nucleomorphin, and at throughout development A. 1991; Full Text PDF PubMed Scopus Google Scholar). The role of CaM in the nucleus is and nuclear CaMBPs have identified in other A.R. Friedberg F. FASEB J. 1997; 11: 331-340Crossref PubMed Scopus Google Scholar). PubMed Scopus Google that one Ca2+-dependent nuclear CaMBPs in but nucleomorphin is the first nuclear CaMBP to be characterized in Furthermore, the first the CaM-binding of a The of nucleomorphin at the nuclear periphery and the in nuclear number in lacking the DEED repeat suggest that protein is in of the Dictyostelium for the Dictyostelium cDNA for the and for on of the

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