THE JOURNAL OF BIOLOGICAL CHEMISTRY Vol. 262, No. 26, Issue of September 15, pp , 1987 Printed in U.S.A.
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1 THE JOURNAL OF BIOLOGICAL CHEMISTRY Vol. 262, No. 26, Issue of September 15, pp , 1987 Printed in U.S.A. Regulation of Biosyntesis of Hypusine in Cinese Hamster Ovary Cells EVIDENCE FOR eif-4d PRECURSOR POLYPEPTIDES* (Received for publication, December 18, 1986) Myung Hee Park From te National Institutes of Healt, National Institute of Dental Researc, Laboratory of Oral Biology arzd Pysiology, Betesda, Maryland Te effects of spermidine depletion and te effects translational modification, step 1; 3) post-translational modof translation inibition on ypusine biosyntesis were ification, step 2. studied in Cinese amster ovary cells. Upon depletion Te rate of ypusine formation parallels te increase in of cellular spermidine by treatment wit DL-a-difluo- protein syntesis in mitogen-treated uman periperal lymrometylornitine for 42 or longer, bot te rate of pocytes (5) and correlates in general wit te rate of cellular deoxyypusine ypusine syntesis and te content proliferation in various mammalian cells (6-8). Te overall of protein-bound ypusine were significantly reduced. regulation of ypusine biosyntesis, altoug not clearly Cycloeximide caused complete inibition of deoxy- understood, may depend upon te rate of syntesis of eif-4d ypusine ypusine syntesis in untreated cells and in cells in wic te spermidine level was reduced to approximately 10% tat of te untreated cells by in- precursor I (Sceme l), te concentration of tis precursor, te level of intracellular spermidine, and/or te activities of te enzymes involved. cubation wit DL-a-difluorometylornitine for 24. Te level of spermidine in mammalian cells can be manip- In contrast, te initial syntesis of deoxyypusine ulated by te use of (9), wic is an irreversible ypusine was not arrested by cycloeximide in cells inibitor of ornitine decarboxylase, a regulatory enzyme in depleted of spermidine by treatment wit DL-a-difluo- te biosyntesis of polyamines (10). Te dependence of te rometylornitine for 42. Te initial rate of deoxy- rate of ypusine syntesis on spermidine concentration as ypusine ypusine production in tese spermidine- been reported in -treated rat epatoma (HTC) cells (8, depleted cells increased 5- to 10-fold wen te cellular 11). Furtermore, te presence of a pool of unmodified eifspermidine level was restored troug addition of tis 4D precursor in tese cells was postulated on te basis of an polyamine to te culture medium. Tese findings sug- immediate increase in te rate of ypusine syntesis following gest tat in control Cinese amster ovary cells and in restoration of cellular spermidine (8). A similar eif-4d precells containing -10% of te control level of spermicursor was also proposed to be present in resting uman dine, deoxyypusine ypusine syntesis occurs durperiperal lympocytes (5). However, no definitive evidence ing or immediately after eukaryotic initiation factor in support of tese proposals as tus far been provided. 4D precursor translation. However, in cells during Te present study was undertaken to gain insigt into te depletion of spermidine, tere is an accumulation of an overall regulation of tis post-translational modification in eukaryotic initiation factor 4D precursor tat contains -treated and untreated CHO cells. Te experiments no ypusine or deoxyypusine, and in tese cells deoxyypusine ypusine syntesis is mainly regulated by described ere provide evidence tat te initial step of postte cellular level of spermidine. translational modification in untreated cells occurs immediately following te translation of eif-4d mrna, wereas in Eukaryotic translation initiation factor 4D (eif-4d) is te only cellular protein tus far known to contain te unusual amino acid ypusine (N -(4-amino-2-ydroxybutyl)lysine) (1). Te biosyntesis of ypusine occurs by a novel posttranslational event in wic te 4-aminobutyl moiety of te polyamine spermidine is transferred to te eamino group of a specific lysine residue of an eif-4d precursor to form deoxyypusine and in wic te deoxyypusine residue of tis polypeptide is subsequently ydroxylated (2-4). Tus te biogenesis of eif-4d may be divided into tree stages as sown in Sceme 1: 1) Translation of eif-4d mrna; 2) post- * Te costs of publication of tis article were defrayed in part by te payment of page carges. Tis article must terefore be ereby marked advertisement in accordance wit 18 U.S.C. Section 1734 solely to indicate tis fact. Te abbreviations used are: eif-4d, eukaryotic initiation factor 4D; CHO, Cinese amster ovary;, DL-a-difluorometylornitine; HTC, epatoma tissue culture spermidine-deprived cells, te post-translational modification (step 1 in Sceme 1) is repressed and eif-4d precursor I, wic contains no ypusine or deoxyypusine, accumulates. In tese cells, wic contain a pool of eif-4d precursor I, spermidine appears to be te major factor governing te rate of deoxyypusine ypusine biosyntesis troug control of modification step 1 in Sceme 1. Recently Duncan and Hersey (12) proposed a coupled translation/ypusine modification of eif-4d in HeLa cells. Our observations in CHO cells provide new information on te relationsips between te translation and te two steps of post-translational modification and tus contribute a furter understanding of te regulation of ypusine syntesis. EXPERIMENTAL PROCEDURES CHO cells WTB were kindly supplied by Dr. April R. Robbins (National Institutes of Healt). was a gift from Merrel Dow Researc Center. [terminal metylene-h]sperrnidine.3 HCI (-25 Ci/mmol) was purcased from DuPont-New England Nuclear; cycloeximide from Sigma. Oter materials, reagents, and te general procedures for cell culture, radiolabeling, and ion excange croma-
2 Regulation of Hypusine Biosyntesis Modification Modification eif-4d Tmnslation elf-4d Step 1 ef4d Step 2 df4d mrna Precursor I Precursor II tograpy ave been described in previous publications (2-4, 13). Specific details of eac experiment are given in te Figure and Table legends. RESULTS Te data presented in Fig. 1 sow tat te depletion of cellular spermidine by treatment wit causes a reduction in te content of protein-bound ypusine. Wen CHO cells were treated wit a 4 mm level of, cellular putrescine dropped to below a detectable level witin 24. Spermidine was reduced to about 10% of tat of untreated cells at 24 and was not detectable after 48 of treatment wit (Table I). Te content of protein-bound ypusine was lowered by -20% after 24 but dropped to approximately 30% of te value of untreated cells between 48 and 72 of treatment (Fig. 1). Tis reduction in protein-bound ypusine may result from decreased ypusine syntesis, from increased degradation of eif-4d, or from canges of bot. To date, te effect of polyamine depletion on te turnover of eif-4d as not been precisely determined. However, te marked repres- (Deoxyypusine Form) (Lysine Form) Form) (Hypusine SCHEME 1 * untreated sion of te post-translational modification upon spermidine depletion as sown in Fig. 2C suggests tat decreased syntesis may be mainly responsible for te reduction in proteinbound ypusine. Te reduction of ypusine was not as pronounced as tat of spermidine in tese -treated cells, presumably because only a minute portion of te total cellular spermidine is used for ypusine production and because te alf-life of eif-4d is relatively long (8). Te relationsips between cellular spermidine levels and te initial rates of modification (step 1 in Sceme 1) were assessed in untreated cells and in tose treated wit (Fig. 2). In newly modified protein, tat wic contains radioactivity provided troug a structural contribution from [3H]spermidine, te transient intermediate ['Hldeoxyypusine was seen in addition to ['Hlypusine. Parentetically, in te digest of total cellular proteins, only ypusine was detected wit te use of te fluorometric metod (Fig. l). Tis is te case because te quantity of te transient intermediate deoxyypusine is very small (0.1-5 pmol/mg protein) compared to total ypusine ( nmol/mg protein). Te relative amounts of [3H]ypusine and ['H]deoxyypusine in newly modified protein varied in untreated and treated cells (Table 11). Te percentages of [3H]deoxyypusine in [3H]deoxyypusine ['Hlypusine at after addition of [3H]spermidine were -14.5% in untreated cells (Table 11, part A), -4% in cells pretreated wit for 42 % I TIME (l FIG. 1. Te total content of protein-bound ypusine in un- treated (0) and -treated (A) CHO cells. Cells were plated and treated as described in te legend to Table I. Tricloroacetic acid precipitates of cells from dises were ydrolyzed in 6 N HCl, and ypusine in te digests was partially purified by ion excange cromatograpy on Bio-Rex 70 as previously described (4). Hypusine content in te partially purified fraction was determined by ion excange cromatograpy and fluorometric detection described as (4, 13). TABLE I Polyamine content of untreated and -treated CHO cells Cells were plated in 100-mm dises at approximately 1 X lo6 cells/ dis in te a-modification of Eagle's medium supplemented as described (3). After l day, (4 mm) was added. At 24, 48, and 72 after addition, cells were wased and arvested as described (3). To te pellet of cells from one dis, 0.2 ml of 5% tricloroacetic acid was added. Te polyamines in 0.1 ml of te acid supernatant were measured wit te use of fluorometric detection after teir ion excange cromatograpic separation employing te tree-buffer system described earlier (13). Cell treatment Incubation time Untreated 0 Untreated 24 Untreated 48 Untreated Putrescine Spermidine Spermine nmollmg protein t <O.l co <o. 1 < A B C D DFMoUr*SPD HOURS MER *DOITION OF ['HI SPERMIDINE FIG. 2. Te rate of deoxyypusine ypusine syntesis in untreated and -treated CHO cells. Cells were preincubated in te absence of for 42 (A) and in te presence of 4 mm for 24 (B) and 42 (C). At te end of te preincubation period, [3H]spermidine(5 pci/ml, -0.2 p was ) added togeter wit (A) or witout (0) cycloeximide (100 pg/ml). To tose cells pretreated wit for 42, additions of ['Hlspermidine and unlabeled spermidine (2.5 p were ) also made togeter wit (A) or witout (0) cycloeximide (D). Te intracellular polyamine content, te polyamine specific radioactivities, and te protein-bound radioactivities in ypusine and deoxyypusine were measured. Te levels of newly formed deoxyypusine ypusine were estimated on te assumption tat te specific radioactivities of tese amino acids are directly related to tat of cellular spermidine. Te specific radioactiv- ity of intracellular spermidine canges continuously after addition of ['Hlspermidine. In te following calculation te spermidine-specific radioactivities employed were tose measured at te middle of te incubation periods. Te values for newly formed protein-bound deoxyypusine ypusine were estimated wit te use of te following expression: Newly formed protein-bound deoxyypusine ypusine (pmol/mg protein) = cpm (deoxyypusine ypusine)/(% X SRA X P), were SRA is spermidine specific radioactivity (cpm/pmol) and P is protein content (mg). Te factor % is used because only one of te two labeled metylenes from spermidine is incorporated into ypusine (2, 24). Te abbreviations used are: CH, cycloeximide; SPD, spermidine.
3 Regulation Biosyntesis of Hypusine TABLE I1 Distribution of deox.v,vpusine and ypusine Cells were treated as described in te legend to Fig. 2, A-D. Te quantity of newly formed deoxy-ypusine and -ypusine were estimated as described in te legend of Fig. 2 after ion excange cromatograpic separation of tese amino acids. In parenteses are given te percentages of eac of te two components in newly formed deoxy?rpusine ypusine C a- 7 Incuation Cell treatment,,musine Hvpusine.ypusine vpusine.. time - A. Untreated R. 24 C. 42 D. 42 SPD Deoxv- Deoxv- prnol/rne protein 0.22 (14.5) 0.38 (6.0) 0.23 (20.9) 0.42 (8.0) 0.05 (4.0) 0.06 (3.0) 5.25 (70.0) 5.20 (34.7) - (06) (85.5) 6.0 (94.0) 0.87 (79.1) 4.80 (92.0) 1.2 (96.0) 2.0 (97.0) 2.25 (30.0) 9.80 (65.3) Untreated D 31 E DF MO Cycloeximide F mrh]leucine (Table 11, part C), a n d -70% in cells initially depleted of I\rH]Hypusine IrHjDeoxyypusine and ten restored wit spermidine (Table 11, part D ). T e percentages of ["Hldeoxyypusine decreased wit incubation time and were lower tan 5 5 after 24 (not sown) in all cases. In spite of te inerent tecnical limitations involved in te accurate determination of ypusine and deoxyypusine from radioactivity measurements as described in te legend 2, teestimatedratesinuntreatedexponent.ially offig. growing CHO cells are in fair agreement wit tose values (1-2 pmol/mg protein/) previously reported for CHO cells UNTREATED CYCLOHEXIMIDE and HTC cells (6, 8). Te rate of deoxyypusine ypusine FIG. 3. Comparison of radiolabelingof eif-4d fromunsyntesis declined only sligtly after 24 of treatment treated and -treated CHO cells. Untreated cells were in(compare A and R in Fig. 2, O ).Tus, it appears tat tereis cubated wit [.'H]leucine (20 pci/ml) and ["Hlspermidine (5 pci/ml) no significant inibition of eiter te translation of eif-4d in medium containing approximately5%of te normal level of leucine mrna or te modification of eif-4d precursor I (Sceme 1) for 2 ( A and 11). Cells pretreated wit for42 were incubated under te same conditions,except tat unlabeled spermiuptotispoint.markeddepression of deoxyypusine ) added togeterwit [:'H]leucineand ["Hlspermidine ypusine formation was found to occur after 42 at te time dine (2.5 p was wen cellular spermidine was depleted (compare A and C in ( R and E ). -pretreated cells were also incubated under tese in te presence of cycloeximide (100 pg/ml) ( C and F ). Fig. 2, 0 ).Tis reduction in modification step 1 (Sceme 1) conditions Wole cell proteins (-200 p g ) were analyzed by two-dimensional is probablyresponsiblefortedecreaseinprotein-bound polyacrylamide gel electroporesis (23). Radiofluorograms of portions -ypusine (Fig. 1 ) and te accumulationof eif-4d precursor I of te gels surrounding te area occupied by eif-4d are sown. Te position of elf-4d is denoted by te solid arrou's. Te portionsof te (Figs. 2 and 3 ) in -treated cells. Inibition of translation by cycloeximide caused te com- gels occupied by eif-4d in A-C were excised, te protein in eac gel plete arrestof new syntesis of deoxyypusine ypusine in piece was ydrolyzed in acid, and te amounts of radioactivity in leucine and deoxyypusine ypusine were measured (11-F)after untreated CHO cells (Fig.2 A, A),and also in cells pretreated ion excange cromatograpic separation. wit for24 (Fig. 2R,A).Tis effect by cycloeximide was seen in cells from te early to telate exponential stage dine content (, 24 ), cells virtually depleted of sperof growt irrespectiveof cell densities (not sown). Te failure midine(,42)sowedessentiallynoinibition of of untreated cells and cells wit reduced spermidine content production of deoxyypusine ypusine by cycloeximide ( 24 ) to form ypusine in te presence of cycloeximide probably results from te lackof substrate protein eif- (Fig. 2C, A). Wereas te addition of exogenous spermidine 4D precursor I (Sceme l),rater tan from inibitionof t e (2.5 P M ) did not cause canges in te rate of deoxyypusine ypusine syntesis in control cells (not sown), replenisenzymes involved. Certainly, te enzymes involved in ypusine production are functional in te presence of cycloexi- ment of tis polyamine to te control level in spermidinemide (Fig. 2, C and D, A).Tus te indication of te lack of depleted cells (, 42 ) by additionof 2.5 P M unlabeled spermidine (8) togeter wit ["Hlspermidine, caused a 5- to eif-4dprecursor I accumulation supports te notion tat eif-4d precursor I undergoes post-translational modificat.ion 10-fold elevation of te initial rate of syntesis of deoxyypusine ypusine(compare C and D in Fig. 2, 0 ). T e during or immediately following translation in control cells finding of no apparent inibition by cycloeximide at and even in cells wit reduced spermidine content (, 24 ). Furtermore, te complete arrest of radiolabeling of (Fig. 2 0, A) is probably due to te small amount of eif-4d eif-4d by cycloeximide (Fig. 2, A and R, A) suggests tat precursor I newly translated during tis period compared to ypusine is produced only de nouo in eif-4d precursori and wat may be a pre-existing pool of precursor 1. Te partial tat tere is no patway for excange or turnover of te 4- inibition seen at 5 (Fig. 211, uertical broken arrow) is likely amino-2-ydroxybutyl moiety in te ypusine residue of eif- teresult of arrest of eif-4dprecursoritranslationby cycloeximide over te incubation period of 5. Certainly, 4D. In contrast to control cells and cells wit. reduced spermi- te cycloeximide resistant labeling of deoxyypusine y-
4 pusine substantiates te existence of a pool of eif-4d precursor I in te spermidine-depleted cells. Evidently, te accumulation of tis precursor occurred wen te rate of modification (step 1 in Sceme 1) dropped below tat of te translation of eif-4d mrna as a result of reduction of cellular spermidine from -10% (, 24 ) to an undetectable level (, 42 ). Te extent of eif-4d precursor I accumulation during te period between 24 and 42 of treatment may be estimated as approximately 9 pmol/mg of protein from te maximum value of cycloeximide-resistant syntesis of deoxyypusine ypusine (Fig. 2D, vertical solid arrow). Additional evidence for accumulation of eif-4d precursor I in spermidine-deprived cells was provided by direct comparison of labeling of [3H]deoxyypusine [3H]ypusine and ['HH]leucine in eif-4d from untreated CHO cells wit tat from cells pretreated wit for 42. Labeling was carried out for 2 wit 3H-labeled spermidine and 3H-labeled leucine (Fig. 3). Cold spermidine (2.5 p was ) added to cells pretreated wit (42 ) togeter wit te two radiolabeled compounds in order to maintain te specific radioactivity of te spermidine pool of tese cells comparable to tat of control cells. Bot [3H]deoxyypusine and [3H]ypusine were found in te spots indicated by te solid arrows in essentially te same ratios as given in Table I1 (A and D). Te comparison of D and E in Fig. 3 reveals tat te post-translational modification represented by radiolabeling in [3H]deoxyypusine ['Hlypusine was -10 fold greater in cells pretreated wit (42 ) tan in control cells, wile te rates of syntesis of eif-4d precursor I represented by ['Hlleucine incorporation were similar. Furtermore, cycloeximide wic caused te complete inibition of [3H]leucine incorporation into eif-4d, did not block te post-translational formation of [3H]deoxyypusine [3H]ypusine in cells pretreated wit for 42 (Fig. 3F). No radiolabeling of eif-4d was observed wen control cells were incubated wit Regulation Biosyntesis of Hypusine precursor I in spermidine-deficient cells, we ave tus far ["Hlspermidine and [3H]leucine in te presence of cycloexi- failed to detect eif-4d precursor I protein after separation of mide (not sown). Tus a rapid modification of a pool of eif- cellular proteins by two-dimensional gel electroporesis. Tis 4D precursor I accumulated during spermidine depletion must may be due to te small quantity of tis precursor, % ave occurred upon replenisment of tis polyamine in te of te total cellular protein, and te limited resolution of our absence (Fig. 3E) or presence (Fig. 3F) of cycloeximide. Te two-dimensional gels. Enricment of tis protein fraction and post-translational modification independent of new transla- use of specific antibodies may provide te means for direct tion seen in E and F of Fig. 3 is consistent wit te data given identification of tis precursor protein. in Fig. 20 and strongly supports te presence of a pool of Te pysiological significance of te decreases in te bioeif-4d precursor I in spermidine-depleted cells. syntesis and content of protein-bound ypusine, and of te DISCUSSION Te data presented in tis paper provide strong evidence tat te post-translational modification of eif-4d precursor I (step 1 in Sceme 1) normally occurs concomitant wit or immediately after translation of eif-4d mrna in control CHO cells and also in cells wit approximately one-tent of teir normal spermidine content (, 24 ). A coupled translation/ypusine modification as been proposed by Duncan and Hersey (12) on te basis of te effects of translation inibition in HeLa cells on te incorporation of radioactivity from ["Hlspermidine into eif-4d. However, we ave detected te accumulation of a small amount of deoxyypusine-containing eif-4d precursor I1 in control CHO cells and in cells wit reduced spermidine content (A and B, respectively, in Table 11). Tus it appears tat altoug deoxyypusine syntesis is coupled to translation, immediate ydroxylation may not occur following te initial step of modification. Furtermore, we ave found conditions under wic te translation and te post-translational modification step 1 (Sceme 1) can be uncoupled. Our data suggest tat in cells wic are virtually depleted of spermidine, deoxyypusine syntesis is no longer coupled to translation, te eif-4d precursor I tat contains no deoxyypusine or ypusine accumulates and, upon replenisment wit spermidine, rapid modification of preformed eif-4d precursor I can occur. It is obvious from te data in Fig. 2 tat te rate of modification (step 1 in Sceme 1) is significantly reduced wen spermidine is depleted. Weter cellular polyamines regulate te translation of eif-4d mrna and its gene expression is not known. However, it may be concluded tat te accumulation of eif-4d precursor I can result from te differential effects of spermidine depletion on te translation and te modification (step 1 in Sceme 1). In te cells containing a pool of eif-4d precursor I (42 preincubation wit, C and D in Fig. 2) spermidine appears to be te major factor determining te rate of deoxyypusine ypusine formation (modification step I in Sceme 1). Te spermidine concentration dependence of ypusine syntesis in rat epatoma cells was previously reported by Gerner et al. (8). It is not clear at present weter te effect of cellular spermidine is exerted at te level of substrate concentration or at te level of activities of te enzymes involved or bot. It is obvious from te data of Table I1 tat bot radiolabeled deoxyypusine and ypusine are detected in te early times after addition of [3H]spermidine. Altoug te quantity of deoxyypusine is small compared to te total protein-bound ypusine (Table I1 and Fig. I), te levels of deoxyypusine in newly modified protein are iger in te cells wit te iger initial rates of modification (step I, Sceme 1). Tis increased accumulation of unydroxylated amino acid may result from a relatively stable rate of ydroxylation irrespective of te large increase in initial syntesis of deoxyypusine. Alternatively, deoxyypusine ydroxylation may also be regulated by te level of cellular polyamines and in an independent manner. Tis possible regulation is currently being investigated. In spite of te strong evidence for accumulation of eif-4d accumulation of eif-4d precursor I in -treated cells is not known. Depletion of putrescine and spermidine by leads to depression of total cell protein syntesis in HTC cells (14) and in mitogen-activated lympocytes (15) and causes te inibition of growt in various mammalian cells (16-19). However, te mecanism by wic polyamines contribute to te regulation of cellular proliferation is not clearly under- stood. In cells treated wit, or in mutant cells defective in polyamine syntesis, te marked inibition of replication is delayed by 1 to 3 generations after te depletion of putrescine and spermidine (16, 18, 20, 21). On tis ground it was speculated tat te inibition of proliferation may not be a direct consequence of polyamine depletion, but rater tat polyamines may participate in te biogenesis of some cellular component(s) tat is required in te replication (18). Since neiter te function of eif-4d in eukaryotic protein syntesis (22) nor te role of ypusine in tis factor as been elucidated, it is as yet premature to attribute inibition of cellular proliferation to a decrease in ypusine. In a recent report, Duncan and Hersey (12) suggest tat canges in eif-4d ypusine modification or abundance are not correlated wit translation repression in HeLa cells by serum depletion, eat sock, or
5 12734 Regulation Biosyntesis of Hypusine ypertonic sock. Altoug normally, eif-4d precursor is largely modified to contain ypusine, our results sow tat te modification (step 1, Sceme 1) is regulated in treated cells were cellular spermidine is drastically reduced. In tis system, te modification may play a critical role in te modulation of protein syntesis and cellular proliferation. Te isolation of eif-4d precursor I from spermidine-deficient cells would provide te first step towards an understanding of te role of ypusine. Possession of tis unmodified protein is certainly essential for in vitro studies of te mecanism of biosyntesis of deoxyypusine and ypusine and its regulation. Acknowledgments-I am grateful to Dr. J. E. Folk for is advice and encouragement trougout tis work; I also tank Dr. H. L. Cooper for te two-dimensional gel electroporetic separations. Addendum-Since te submission of tis paper, we ave obtained more direct evidence for accumulation of eif-4d precursor I in spermidine-depleted CHO cells. Wen tese cells ( for 42 ) were incubated for 6 in te presence of [3H]lysine, no labeled eif- 4D (ypusine form, M, -18,000; PI -5.3) was detected by ig resolution two-dimensional gel electroporesis. Instead, a new radiolabeled cellular protein (M,-18,000; PI -5.1) wic migrated at a position predicted for eif-4d precursor I was seen. Peptide mapping studies are underway in an effort to confirm te identity of tis protein as eif-4d precursor I. REFERENCES 1. Cooper, H. L., Park, M. H., Folk, J. E., Safer, B., and Braverman, R. (1983) Poc. Natl. Acu. Sci. U. S. A. 80, Park, M.H., Cooper, H. L., and Folk, J.E. (1981) Proc. Natl. Acad. Sci. U. S. A. 78, Park, M. H., Cooper, H. L., and Folk, J. E. (1982) J. Biol. Cem. 257,721? Park, M. H., Liberato, D. J., Yergey, A. L., and Folk, J. E. (1984) J. Biol. Cem. 259, Cooper, H. L., Park, M. H., and Folk, J. E. (1982) Cell 29, Torrelio, B. M., Paz, M. A., and Gallop, P. M. (1984) Erp. Cell Res. 154, Cen, K. Y. (1983) Biocin. Biopys. Acta 756, Gerner, E. W., Mamont, P. S., Bernerdt, A,, and Sat, M. (1986) Biocem. J. 239, Metcalf, B. W., Bey, P., Danzin, C., Jung, M. J., Casara, P., and Vevert, J. P. (1978) J. Am. Cem. SOC. 100, Tabor, C.W., and Tabor, H. (1984) Annu. Reo. Biocem. 53, Gerner, E. W., and Mamont, P. S. (1985) Recent Progress in Polyamine Researc (Selmelci, L., Brosnan, M. E., and Seiler, N., eds) pp , Akademiai Kiado, Budapest 12. Duncan, R. F., and Hersey, J. W. B. (1986) J. Biol. Cem. 261, Folk, J. E., Park, M. H., Cung, S. I., Scrode, J., Lester, E. P., and Cooper, H. L. (1980) J. Biol. Cem. 255, Rudkin, B. B., Mamont, P. S., and Seiler, N. (1984) Biocem. J. 217, Holttii, E., and Hovi, T. (1985) Eur. J. Biocem. 152, Mamont, P. S., Ducesne, M-C., Grove, J., and Bey, P. (1978) Biocem. Biopys. Res. Commun. 81, Oredsson, S., Aneus, S., and Heby, 0. (1980) Biocem. Biopys. Res. Commun. 94, Holtta, E., Pojanpelto, P., and Janne, J. (1979) FEBS Lett. 97, Seyfried, C. E., and Morris, D. R. (1979) Cancer Res. 39, Steglic, C., and Sceffler, I. E. (1982) J. Biol. Cem. 257, Pojanpelto, P., Virtanen, I., and Holtta, E. (1981) Nature 293, Tomas, A. A. M., Benne, R., and Voorma, H. 0. (1981) FEBS Lett. 128, O Farrell, P. H. (1975) J. Biol. Cem. 250, Park, M. H., and Folk, J. E. (1986) J. Biol. Cem. 261,
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