Emr-2's genes that specify altered S20 protein (S20*) and emetine
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1 Poc. Natl. Acad. Sci. USA Vol. 76, No. 1, pp , Januay 1979 Genetics Emetine esistance in Chinese hamste cells is linked genetically with an alteed 40S ibosomal subunit potein, S20* (somatic cell genetics/two-dimensional gel electophoesis/mitotic segegation/hybid cells) D. BOERSMA, S. M. MCGLL, J. W. MOLLENKAMP, AND D. J. ROUFAt Division of Biology, Kansas State Univesity, Manhattan, Kansas 6606 Communicated by Chales D. Michene, Octobe 11, 1978 ABSTRACT Em-2 is an emetine-esistant (Em) Chinese hamste ovay cell mutant that contains a single electophoetically alteed ibosomal potein, a component of its 40S ibosomal subunit [Boesma, D., McGill, S., Mollenkamp, J. & Roufa, D. J. (1979) J. Biol. Chem. 24, in pess]. This epot descibes a genetic expeiment designed to test linkage between the genes that specify the alteed ibosomal potein, S20*, and emetine esistance in Em clones that segegated fom cultues of Em-2 cells hybidized with emetine-sensitive cells. The data descibed indicate that Em and S20* phenotypes ae due to mutations linked to the same chomosome in the Chinese hamste genome; most likely they ae due to the same mutation. The data also confim ealie speculations by othes that the Em locus in Chinese hamste cells is hemizygous. Seveal Chinese hamste cell mutants that expess genetically alteed ibosomal functions have been isolated in ou laboatoy. Within this collection ae nine mutagen-induced clones whose ibosomes ae esistant to emetine (Em), an alkaloid dug inhibito of potein biosynthesis (1). We used two-dimensional polyacylamide gel electophoesis to analyze 72 poteins extacted fom Em mutants' ibosomes. We obseved that only one ibosomal potein pepaed fom mutant clone Em-2 was alteed in a manne detectable by ou assay. The alteed potein, S20*, a component of the 40S ibosomal subunit, diffes fom wild-type S20 potein in its electophoetic migation at ph. S20 and S20* migated with identical mobilities in buffe containing sodium dodecyl sulfate (i.e., appeaed to possess the same molecula weight) (1). These obsevations wee consistent with S20* having aisen by a point mutation. The identification of an alteed 40S ibosomal subunit potein fom an Em clone ageed with othe investigatos' assignment of emetine esistance in Chinese hamste cells to the 40S ibosomal subunit (2) Ṫhee genetic models could account fo the elationship between the alteed ibosomal potein S20* and Em-2's Em phenotype: (i) Emetine esistance might be independent of the alteation in S20 potein. (ii) The mutation esponsible fo emetine esistance might affect a gene coding fo a potein that modifies S20 potein. S20* thus might be the nonmodified, electophoetically distinguishable pecuso to nomal S20. (iii) The stuctual gene that codes fo S20 potein might contain a mutation esponsible fo both S20* and the mutant's esistance to emetine. The electophoetic and genetic expeiments descibed in this epot wee designed to investigate the elationship between S20* potein and the Em phenotype of clone Em-2. We fused a deivative of Em-2 with emetine-sensitive (Ems) Chinese hamste cells and selected seveal appoximately tetaploid hybid clones. Spontaneous Em mitotic segegants wee isolated fom hybid clones, and poteins fom the 40S ibosomal The publication costs of this aticle wee defayed in pat by page chage payment. This aticle must theefoe be heeby maked "advetisement" in accodance with 18 U. S. C solely to indicate this fact. 41 subunits of hybid and segegant clones wee analyzed by two-dimensional polyacylamide gel electophoesis. By these expeiments, we tested the chomosomal linkage between Em-2's genes that specify alteed S20 potein (S20*) and emetine esistance. MATERALS AND METHODS Mateials. Amethoptein, thymidine, and 6-thioguanine (6-TG) wee puchased fom Sigma. Hypoxanthine was a poduct of P-L Biochemicals. Polyethylene glycol-6000 (PEG-6000) was a Bake eagent. The souces of all othe mateials have been descibed befoe (1). Tissue Cultue. Oigins and gowth chaacteistics of the emetine-esistant Chinese hamste ovay cell clone Em-2 (1) and the thymidine-kinase-deficient (TK-) mutant Chinese hamste lung (CHL) cell (V79) clone (3, 4) have been descibed. Clones (Em-2/6-TG)_1 and (Em-2/6-TG)-2 ae two 6-thioguanine-esistant (6-TG) deivatives of Em-2 that wee obtained by teating Em-2 with ethyl methanesulfonate and selecting double mutants in 2,uM 6-TG (). These 6-TG clones wee used to geneate Em-2-Ems hybid clones unde fully selective cultue conditions (see below). Hybid clones wee obtained by fusing mutant paental clones (Em-2/6-TG)-1 and -2 with , Ems/TK-. Cells wee fused by cocultivating 106 cells of each paental clone in a 60-mm dish and teating them with 0% (wt/wt) PEG-6000 (6). Hybid clones wee selected in medium containing 100,gM hypoxanthine,,tm amethoptein, and 20 1,M thymidine (HAT) (). Subsequently Em clones that segegated fom hybid clones wee selected by adding 0.2,uM emetine to cultue media. The kayotypes of hybid and segegant clones wee analyzed as descibed peviously (4). Chinese Hamste Cell Ribosomes and Ribosomal Poteins. Pocedues fo puifying Chinese hamste cell ibosomal subunits fom polyibosomes have been descibed (1, 7). The 80S ibosomes wee dissociated in buffe that lacked Mg2, and 40S and 60S ibosomal subunits wee isolated by sucose gadient centifugation. The 40S ibosomal subunits pepaed by this pocedue contained less than 1% coss-contamination of 60S subunits. Extaction of ibosomal poteins and thei analysis by two-dimensional polyacylamide gel electophoesis also ae descibed in detail elsewhee (1). Abbeviations: CHO, Chinese hamste ovay cell line; CHL, Chinese hamste lung cell line (V79); PEG, polyethylene glycol; Em, emetine esistance o esistant; Ems, emetine sensitivity o sensitive; TK-, thymidine kinase-deficient; 6-TG, 6-thioguanine; 6-TG and 6-TGs, esistance and sensitivity to 6-TG; HAT, medium containing 100AM hypoxanthine, AM amethoptein, and 20 AM thymidine; S20, a 40S ibosomal subunit potein found in Ems CHO and CHL cells; S20*, an alteed fom of S20 potein found in the clone Em-2. t To whom all coespondence should be addessed.
2 416 Genetics: Boesma et al. RESULTS A two-dimensional gel electophoesis patten of 40S ibosomal poteins fom the mutant clone Em-2 is illustated in Fig. 1. S20* potein chaacteistic of Em-2 (1) is indicated in the figue. Wild-type S20 potein seen in contol two-dimensional gels also is dawn in the figue slightly to the ight of S20*. A efeence line useful fo intepeting the gel pattens that follow is defined accoding to its elationship with poteins nea the position of S20. The ectangle within the patten defines the specific aea of simila gels enlaged fo close examination (Figs. 3 and 4). Note that the positions of S20* potein and of wild-type S20 potein in the second dimension (the sodium dodecyl sulfate dimension) indicate thei simila molecula weights, about 1,000 (1). Migations of S20 and S20* in the ph uea dimension (i.e., the fist-dimension electophoesis) diffeed only slightly, and this diffeence appeaed to be due to a decease in the net positive chage chaacteistic of wildtype S20 potein. Expeimental Plan. To examine the genetic elationship between emetine esistance and the alteed 40S ibosomal subunit potein S20*, we pefomed the expeiment outlined in Fig. 2. As descibed by Ruddle (8), hypeploid animal cell hybid clones spontaneously lose chomosomes in appoximately a andom ode duing mitotic gowth. As a consequence, nonlinked genetic loci often segegate in cultues of somatic cell hybids. Thus, if a hybid cell is heteozygous fo two genes, lack of mitotic segegation between alleles making these genes can povide evidence fo thei genetic linkage. n hybid clones with Em/Ems, S20*/S20 genotypes, spontaneous loss of the chomosome beaing the Ems allele should yield daughte clones that expess the ecessive Em phenotype (2). f all spontaneous Em segegants also expess only the S20* ibosomal potein, then the genes that specify Em and S20* ae likely to be located on the same chomosome. Altenatively, if the Em and S20* phenotypes segegate independently, then they ae not linked and cannot be attibuted to the same chomosomal locus. n addition, because paental cells used to geneate hybids (Em-2/6-TG) contained the X-linked genetic make fo 6-thioguanine esistance (9), if the Em and 6-TG phenotypes ae expessions of linked genes, then the locus specifying esistance to emetine also must be X-linked. Because 6-TG Chinese hamste cells cannot gow in HAT medium (), Poc. Natl. Acad. Sci. USA 76 (1979) Em'-2 (n=21) //Ethyl methanesulfonate 6- TG (n=21) Em'-2/6-TG x Em'/TK- (n=18) PEG HAT HYBRD CLONES Em-2 6-TG TK (n 39) Em' 6-TG' TK- Emetine / \ Emetine E] HAT Em-SEGREGANTS ( n- 38): Possibilities: a)em a 6-TG linked: Em TG TK 0 TKb) Em a 6-TG' unlinked: Em- 2 6-TG' TK 0 6-TG' TK- FG. 2. Segegation of emetine esistance fom Em/Ems Chinese hamste cell hybids. if Em is X-linked, Em segegant clones should be HATS (sensitive to HAT medium). Em/EmS Hybid Clones. Two 6-TG deivatives of Em-2, (Em-2/6-TG)-1 and (Em-2/6-TG)-2, wee used to geneate hybid clones by fusion with the Ems/TK- clone, Hybid clones wee selected in HAT medium on the basis of the paental lines' complementay HATS mutations (6-TG and TK-) (10). Hybid clones aose at high fequency (-9 X 10-3) in cultues that contained mixtues of both 6-TG and TKpaental cell types (Table 1). Cultues that contained only 6-TG cells o only TK- cells gave ise to HAT-esistant colonies (HAT) with much lowe fequency (<6 X 10-6). The few HAT clones deived fom cultues that contained only (Em- 2/6-TG)-2 o only did not eflect hybid fomation, in that these clones possessed the same numbe of chomosomes as thei paents-i.e., 21 fo (Em-2/6-TG)-2 and 18 fo (data not shown). Thus, the HAT colonies deived fom cultues of (Em-2/6-TG)-2 o appeaed to be due to evesion of the paental cells' HATs mutations. Seveal HAT hybids wee isolated and ecloned fom mixtues of both Em-2/6-TG paents and n the following expeiments hybids designated A and B wee deived "... : 'W", ~' t * >- 1-D & L-..? C2-U.w *: FG. 1. Two-dimensional gel patten of 40S ibosomal subunit poteins fom Em-2. This gel, stained with Coomassie blue, contained 120,g of Em-2 40S subunit poteins. Migation in the fist dimension on a tubula 4% polyacylamide gel containing 8 M uea at ph.0 was fom left to ight as displayed in the figue. The second-dimension electophoesis was fom top to bottom on a 1% polyacylamide slab gel in buffe containing sodium dodecyl sulfate. The locations of S20*, the potein alteed in Em-2, and wild-type S20 (dawn in outline) in compaable gels of the paental CHO cell line's 40S ibosomal subunit poteins ae both indicated in this figue.
3 Table 1. Hybidization of Em-2/6-TG and Ems/TKK Chinese hamste cells Paental clones HAT hybid fequency, mean ± SD (Em-2/6-TG)-1 and Ems/TK ± 0.9 X 10-3 (Em-2/6-TG)-2 and Em8/TK X 10-3 (Em-2/6-TG)-1 and (Em-2/6-TG)-2 <2 X 10-6 (Em-2/6-TG)-1 and (Em-2/6-TG)-1 <2 x 10-6 (Em-2/6-TG)-2 and (Em-2/6-TG)-2 2 X 10-6 EmS/TK- and EmS/TK- 6 X 10-6 Mixtues of 106 paental cells of each clone indicated wee inoculated into 60-mm cultue dishes in nonselective medium. Afte one day, the monolaye cultues wee teated with 096 (wt/wt) PEG-6000 fo 60 sec at oom tempeatue (6) and then fed with nonselective cultue medium. Twenty-fou hous afte teatment with PEG, cells wee havested by teatment with typsin and then wee edistibuted to eplicate cultue dishes at densities of 10, 104, o 103 cells pe 100-mm dish in HAT medium. Afte appoximately 7-10 days at 370C, HAT colonies wee fixed with 4% (wt/vol) fomaldehyde, stained with 0.% cystal violet, and scoed. Values in the table epesent the mean ± standad deviations of the -10 dishes fom each fusion mixtue that contained HAT colonies. fom (Em-2/6-TG)-1 and ; those designated C and D, fom (Em-2/6-TG)-2 and The phenotypes of the HAT hybids wee consistant with many of the popeties pedicted in Fig. 2: (i) As anticipated fom the sum of the paental clones' chomosome numbes (Table 2), hybids contained chomosomes. This was consistent with the hypothesis that each hybid clone aose fom the fusion of one 6&TG cell (n = 21) with one TK- cell (n = 18). (ii) The hybids appeaed to contain both the ecessive Em and the dominant, wild-type Em8 genes (2). Each hybid was sensitive to 0.2,uM emetine (i.e., displayed the Ems phenotype). n contast to wild-type Ems lines, which equie mutagenesis to yield Em clones (1, 11), hybid Ems clones spontaneously gave ise to Em deivatives at high fequencies (see Table 3 below). (iii) Hybid clones contained both the oiginal Em-2 gene poduct, S20*, and the wild-type gene poduct, S20. This is illustated in Fig. 3. On the othe hand, 40S ibosomal subunits pepaed fom wild-type Chinese hamste cells contained only the S20 potein (centeed to the ight of the efeence line defined in the figues by its elationship to S1, S12, S1, S24, and S26). 40S ibosomal subunits pepaed fom mutant Em-2 contained only the S20* potein (centeed to the left of the efeence line). Table 2. Genetics: Boesma et al. Kayotype numbes of wild-type, mutant, and hybid Chinese hamste cell clones Clone Numbe of chomosomes, mean ± SEM Wild type: CHO-Ki 21 Mutants: Em Hybids: A B C D 39.2 ±0.2 Kayotype numbes fo the clones listed in the table wee detemined in appoximately 10 chomosome speads (4). S28 Wild q s7 Poc. Natl. Acad. Sci. USA 76 (1979) 417 type st S S9 S13 S14 s - 2O-0.w i S23 Hybid S24 : S26 S30 A -W." *4 S20 S20* * -o 40: Emn 2 44 S20*.i4d Hybi d w- C S 20 S2e-o-,at. ~~~~~~~~~~~~~ FG. 3. Two-dimensional polyacylamide gel electophoesis of 40S ibosomal subunit poteins fom paental and hybid Chinese hamste cells. Enlaged potions of electopheogams, as indicated by the ectangle in Fig. 1 and defined by poteins S7, S8, S9, S10, S13, S23, S28, and S30, ae illustated in this figue. The oientation of the efeence line is descibed in the text. Each gel illustated contained 120 Mug of potein extacted fom puified 40S ibosomal subunits. Em Segegants that Aise fom Ems/Em Hybid Clones. As illustated in Fig. 2, duing gowth in the absence of selective agents, mitotic segegants with an Em phenotype should aise spontaneously in cultues of hybid cell lines. Theefoe, fou hybid clones wee cultued in the absence of dugs fo appoximately 2 cell geneations afte fusion, and the esulting cultues wee tested fo thei content of Em segegants. We scoed Em segegant colonies in medium with and without HAT components (Table 3). All fou hybid clones tested gave ise to Em colonies spontaneously with fequencies that suggested mitotic segegation (12). These fequencies wee simila to fequencies epoted ecently fo the segegation of the Em phenotype fom othe CHO Em-CHL (V79) hybids (13). Futhemoe, the numbes of Em colonies scoed in the pesence and in the absence of HAT components wee appoximately equal. Theefoe, the Em-2 mutation appeaed not to be linked to the 6-TG mutation in the hybid clones (linkage possibility b in Fig. 2). The two 6-TG mutations used in these studies [i.e., as contained in (Em-2/6-TG)-1 and (Em-2/6- TG)-2] segegated with fequencies 10- to 30-fold highe than the Em-2 mutation in cultues of hybid clones A and C (Table 3). Table 3. Segegation of Em and 6-TG clones fom Em-2/6-TG-Ems/TK- hybids Segegation fequencies, mean SD X 10 Hybid Emetine esistance 6-Thioguanine clone -HAT HAT esistance A 4.6 ± ± B 12.4±4.6 4.±1.3 C 4.2± ± ± D 1.8± Hybid clones A-D wee gown fo 2 geneations in the absence of selective agents. Replicate 100-mm cultue dishes wee inoculated with 10 cells of each hybid cell line. Five of these cultues wee teated with 0.2MuM emetine; five wee teated with emetine plus HAT components; and five wee teated with 2MgM 6-TG. Afte 7-10 days at 37 C, the cultues wee fixed with 4% fomaldehyde, stained with 0.% cystal violet, and scoed fo the numbe of clones that suvived to fom visible colonies.
4 418 Genetics: Boesma et at. Table 4. Kayotype numbes of Chinese hamste cell Em mitotic segegants Segegant Numbe of chomosomes, clone mean :: SEM A B B C D Kayotype numbes fo the segegant clones indicated in the table wee detemined in appoximately 10 chomosome speads (4). The expeimental ationale illustated in Fig. 2 equied eithe (i) that Em clones aising by mitotic segegation contain at least one fewe chomosome (the chomosome beaing the Ems allele) than do hybid clones o (ii) that at least pat of the chomosome beaing the Ems allele was inactivated in "segegants" by an unknown pocess. Five independent Em colonies wee isolated fom the fou hybid clones, and the chomosome numbe of each pesumed segegant was detemined (Table 4). n most cases these data wee consistent with a model fo the Em clones' oigins involving loss of at least one complete chomosome. To test fo genetic linkage between the Em-2 mutation and the gene that specifies S20* potein, 408 ibosomal subunits and thei component poteins wee pepaed fom the five Em segegants. These poteins wee analyzed by two-dimensional gel electophoesis. Fou of the segegants' 40S ibosomal subunit potein pattens ae illustated in Fig. 4. n evey Em segegant examined, 40S ibosomal subunits contained only the S20* potein. n no case (five of five tested) did the 40S ibosomal subunits contain wild-type S20 potein. Because both S20 and S20* poteins wee synthesized and assembled into functional 40S ibosomal subunits in hybid cells known to contain genes specifying both poteins, we concluded that the five Em segegants, which expessed only the S20* gene, pobably lost o inactivated the wild-type S20 gene as they aose fom thei paental hybid clones. DSCUSSON The total data on which the mitotic segegation expeiment outlined in Fig. 2 was based ae summaized in Table. As indicated in the table, fou appoximately tetaploid hybid clones each expessed both the wild-type S20 and Em-2 S20* Poc. Nati. Acad. Sa. USA 76 (1979) Table. Cosegegation of emetine esistance with alteed ibosomal potein S20* in Chinese hamste cells Clone Wild type: CHO-K1 Mutants: Em Hybids: A BC D Em mitotic segegants: A-1 B-1 B-2 C-2 D-2 Emetine phenotype S20 S20* Emetine sensitivity (s) and esistance () wee detemined by efficiency of colony fomation in medium containing 0.2,M emetine. The S20 potein phenotypes wee detemined by two-dimensional gel electophoesis of 40S ibosomal subunit poteins (see Figs. 1, 3, and 4). 40S ibosomal subunit poteins, as expected fo Em?/Eme, S20*/S20 heteozygotes. As obseved by othes (2), these hybids with known Em"/Em' genotypes all displayed the Ems phenotype. Five independent Em segegants wee isolated fom these hybid clones, and all five expessed only the S20* potein chaacteistic of Em-2. These segegation data demonstate that the loci that encode mutant ibosomal potein S20* and the Em phenotype ae linked to the same chomosome within the Chinese hamste cell genome. Of the vaious models that might be -used to explain these expeiments, the most diect intepetation suppots model iii descibed in the intoduction-i.e., the s20* and Em genes ae the same. f model i wee coect-i.e., the mutation esponsible fo S20* is independent of emetine-esistance-then ou data equie that the two loci be linked to the same chomosome. nasmuch as loci that specify many ibosomal poteins ae clusteed in the Escheichia colh genome (14), it would not be supising to find that two eukayotic ibosomal genes, s20* and Em, also ae linked. 7 S9 Aaf*. * "-S28 S.3 S1tW -1 _.s..._ C ; i-1 26 &:i...n:.'u :". S2 0ii :JP 44 b~~~~~~~~~~~~~~~~~~~~~~~~ S2O f.., -Seg C i S20.*t._ *.4 4,' *. :1 4 f a_}, FG. 4. The 40S ibosomal subunit poteins fom Em segegant clones. Pattens of wild-type and Em-2 40S ibosomal subunit poteins ae illustated fo compaison. The gel of segegant A- contained 140 pg of 40S ibosomal subunit poteins; the gel of segegant C-2 contained 100i g of potein, and the gels of wild type, Em-2, B-i, and C-1 each contained 120 pug of potein.
5 Genetics: Boesma et al. Whethe o not the Em mutation affects the stuctual gene fo ibosomal potein S20 o the stuctual gene fo an enzyme that modifies an S20 potein pecuso (model ii, intoduction) cannot be deduced with cetainty fom ou data. That appoximately equal amounts of S20 and S20* poteins coexist within hybid cells' polyibosomes (Fig. 3) suggests that the Em-2 mutation does not inactivate an enzyme modifying ibosomal poteins. f it did, enzymes specified by the Ems paents' genes in the hybids would have modified S20* to the matue S20 potein. We have descibed eight othe Em clones isolated fom wild-type CHO and CHL cell lines (1). Although these eight mutants all possess ibosomes that ae esistant to emetine in vito, none of them synthesizes a ibosomal potein, including S20, that could be distinguished fom wild type by two-dimensional gel electophoesis. Howeve, hybidization complementation tests on the complete collection of Chinese hamste Em mutants, pefomed by fusing each mutant in tun with Em-2, indicated that the nine mutants all belong to a single complementation goup (S. M. McGill and D. J. Roufa, unpublished). Thus, all of the Chinese hamste cell Em mutants isolated by us as well as by othes (2) appea to have attained thei dug esistance by a single mechanism. The expeiments descibed above suggest that this mechanism involves 40S ibosomal subunit potein S20 and indicate that this potein foms at least a pat of the ibosomal binding site fo emetine. S20* puified fom hybid cells migated in the sodium dodecyl sulfate-dimension electophoesis slightly faste than S20. This was not obseved when we mixed wild-typ* and Em-2 40S ibosomal subunit poteins pio to electophoesis (1). Thus, the slightly faste migation of S20* when puified fom hybid cells eflected eithe an unexplained aspect of ibosomal potein pocessing in the hybids o a vey small diffeence in the molecula weights of S20 and S20*. On the basis of the migations of standad poteins as well as of neighboing ibosomal poteins, we estimate that S20*s fom all of the hybid clones ae appoximately 100 to 300 daltons smalle than wild-type S20 potein. Although Em-2 was isolated afte teating CHO cells with a mutagen that pomotes pimaily single-base changes in DNA (1), it is possible that the gene fo S20* aose fom the wild-type gene by deletion of one o pehaps two amino acid codons. Also it is possible that the S20* mutation pecluded nomal post-tanslational pocessing of an S20 potein pecuso. Analysis of the typtic peptides and amino acid compositions of S20 poteins puified fom wild-type and Em Chinese hamste cell clones should povide futhe chaacteization of the molecula basis fo emetine esistance. n contast to the heteozygous molecula phenotype of the hybid cell clones, Em-2 cells expessed a single S20 gene Poc. Natl. Acad. Sci. USA 76 (1979) 419 poduct. f Em-2 contained two active genes fo S20 potein (i.e., if it wee functionally diploid at this locus), then, as was obseved in pepaations fom hybid cells, we would have expected to see a mixtue of S20 gene poducts in pepaations of Em-2's 40S ibosomal poteins. t is unlikely that two mutations in Em-2 conveted two CHO cell S20 alleles to S20* independently, because the eight othe Em mutants aleady descibed did not contain an alteation of the S20 potein detectable by electophoesis (1). Theefoe, as suggested by Siminovitch (1), the Em locus in CHO cells appeas to be functionally hemizygous. Because the Em-2 mutation is not X-linked (Table 3), ou expeiments suggest that the Em locus pobably is within one of the seveal unpaied egions of the genome contained in CHO cells (16). f this is tue, CHL cells (V79) also appea to contain the same chomosomal egion in an unpaied configuation, because we have obtained Em mutants with appoximately equal fequencies fom both Chinese hamste cell lines (1). We thank D. T. C. Johnson, Ms. Shaon.Matin, and Ms. Kathy Ogbon fo thei many helpful suggestions and expet assistance in the pepaation of this manuscipt. D.J.R. is the ecipient of Reseach Caee Development Awad GM0024 fom the U.S. Public Health Sevice. This wok was suppoted by Gant GM23013 fom the U.S. Public Health Sevice. This aticle is contibution no A fom the Kansas Agicultual Expeiment Station, Division of Biology. 1. Boesma, D., McGill, S., Mollenkamp, J. & Roufa, D. J. (1979) J. Biol. Chem. 24, in pess. 2. Gupta, R. S. & Siminovitch, L. (1977) Cell 10, Chu, E. H. Y. & Ho, T. (1970) Mamm. Chomosome Newsl. 11, Roufa, D. J., Sadow, B. N. & Caskey, C. T. (1973) Genetics 7, Gillin, F. D., Roufa, D. J., Beaudet, A. L. & Caskey, C. T. (1972) Genetics 72, Davidson, R. L. & Geald, P. S. (1976) Somatic Cell Genet. 2, Haalson, M. A. & Roufa, D. J. (197) J. Biol. Chem. 20, Ruddle, F. H. (1970) Symp. nt. Soc. Cell Biol. 9, Faell, S. A. & Woton, R. G. (1977) Somatic Cell Genet. 3, Littlefield, J. W. (1969) Poc. Natl. Acad. Sci. USA 62, Gupta, R. S. & Siminovitch, L. (1976) Cell 9, Chasin, L. A. (1972) Natue (London) New Biol. 240, Gupta, R. S., Chan, D. Y. H. & Siminovitch, L. (1978) Cell 4, Fiandt, M., Szybalski, W., Blattne, F. R., Jaskunas, S. R., Lindahl, L. & Nomua, M. (1976) J. Mol. Biol. 106, Siminovitch, L. (1976) Cell 7, Woton, R. G. (1977) Somatic Cell Genet. 3,27-4.
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