Persistence of the ten-nucleotide repeat in cbromatin unfolded in urea, as revealed by digestion with deoxyribanuclease I

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1 vlume3 n.7 July 1976 Nucleic Acids Research Persistence f the ten-nucletide repeat in cbrmatin unflded in urea, as revealed by digestin with dexyribanuclease I Mariana Yaneva and Gerge Dessev Institute f Bichemistry, Bulgarian Academy f Sciences, 13 Sfia, Bulgaria Received 7 May 1976 ABSTRACT It is shwn by enzymatic digestin f chrmatin frm rat liver r Guerin ascites tumur (GAT) that treatments, which ablish the 180 base pair repeat, as revealed by digestin with micrcccal nuclease (shearing in salt slutins f medium inic strength, snicatin, fixatin with frmaldehyde in the presence f 5 M urea)? have little effect n the 10 nucletide repeat, bserved in dexyribnuclease I digests. INTRODUCTION Digestin f whle nuclei (1,2) r islated chrmatin (3,4) with micrcccal nuclease (E.C ) in its initial stage generates a series f particles, cntaining discrete sizes f DNA, multiples f 180 base pairs. Digestin with DNAse I prduces single stranded DNA fragments, revealed under denaturing cnditins, which are multiples f 10 nucletides (5). The latter has been assumed t reflect the substructure f nuclesme8 (5). In this cmmunicatin we present evidence that the 10 nucletide repeat persists under cnditins where the 180 base pair, repeat is ablished. MATERIALS AND METHODS "Structured" and- "salt" chrmatins were islated frm rat liver r GAT as described elsewhere (4). DNAse I was a prduct f Wrthingtn, N.J., U.S.A. Micrcccal nuclease was btained frm Sigma. All chemicals were f analytical grade. Urea was deinized by in exchange. Chrmatin (2 AggQ-units/ml in 2 mil TES buffer (ph 7.8), O Infrmatin Retrieval Limited 1 Falcnberg Curt Lndn W1V 5FG England

2 10 um EDTA> 0.1 mm phenylmetftylsulfnyl fluride was digested with micrcccal nuclease in the presence f 0.3 mm CaCl 2 r with DNAse I in the presence f 0.1 mm MgCl 2» In bth cases the incubatin was fr 60 min at 37 C. The reactin was stpped by additin f EDTA in excess. Determinatin f acid sluble prducts and islatin f DNA were perfrmed as described elsewhere (4). DNA was analysed by electrphresis in 2.5% nn-denaturing plyacrylamide gel (4) r in 7.5% gel under denaturing cnditins (6). RESULTS. AND DISCUSSION In a previus wrk we have shwn that n discrete fragmentatin with micrcccal nuclease is bserved in the initial digestin stage (less than 10% acid sluble prducts) f chrmatins prepared by a prcedure which includes hmgenizatin in the presence f 0.15 M and 0.35 M NaCl ("salt" chrmatins) (4). These bservatins, tgether with the results f ther c 0-6 LU 0.4 m I 0 ' 2 CD < DISTANCE MIGRATED (CM) Fig. 1. Electrphretic prfile in 7.5% denaturing plyacrylamide gel f single stranded DNA fragments islated frm "salt" chrmatin, digested with DNAse I as described in Methds t 29% acid sluble prducts. 1762

3 authrs (7,8) suggest that in such chrmatins the peridic structure f 180 base pairs and multiples has been damaged. Fig. 1 shws the electrphretic pattern f DNA frm rat liver "salt" chrmatin, which is identical with the pattern btained with whle nuclei (5) and "structured* chrmatin (6). Similar results were btained with "structured" chrmatin that had been snicated (data nt shwn). DNA islated frm the snicated chrmatin had an average size f 600 base pairs. Digestin f such chrmatins with micr.cccal nuclease t acid sluble material between 5 and 10% failed t reveal discrete fragmentatin f DNA, i.e. the ultrasund was detrimental t the subunit structure f chrmatin. The same chrmatin samples, when digested with DNAse I t acid sluble prducts between 15 and 20% yielded the characteristic pattern f single stranded DNA fragments, multiples f 10 nucletides, identical t that shwn in Fig. 1. These results suggest that the 10 nucletide repeat may exists in the absence f secndary structure in chrmatin. T substantiate this pssibility we carried ut digestins with bth micrcccal nuclease and DNAse I f "structured" chrmatin, fixed with frmaldehyde in the presence f 5 M urea. The unflding effect f 5 M urea n chrmatin is knwn frm the wrk f Bartley and Chalkley (9). It has als been shwn that frmaldehyde fixatin in the presence f urea ablishes the peridic structure f chrmatin, as judged frm x-ray diffractin experiments and electrn micrscpy (10). Structured chrmatin frm Guerin ascites tumur was fixed with frmaldehyde in the presence f 5 M urea as described in (10): chrmatin in 2 mm Tes, 10 um EDTA (ph 7.8) at a cncentratin f 4 ApgQ units per ml was mixed at 0 C with an equal vlume f 10 M urea, previusly deinized and buffered with 2 mm Tes at ph 7.8. After 15 min in ice, 30% frmaldehyde (ph 7.0 adjusted with NaHCO,) was added t a final cncentratin f 1%, the mixture was kept in ice fr 30 min and dialysed against 3 changes f 100 vl. each f 2 mil Tee, 10 um EDTA (ph 7.8) during at least 48 h at 4 C. After this treatment the histnes culd be extracted quantitatively with 0.25 N HgSO^ 1763

4 fr 40 min at 0 C, but they failed t enter 15% urea-acetic acid gel (11). If fixatin was carried ut with 10% frmaldehyde in the presence f 5 M urea, the histnes became unextractable under the same cnditins, but this did nt affect the digestin results. Fig. 2 A shws the nrmal micrcccal nuclease digestin pattern f untreated chrmatin, cnsisting f discrete fragments, multiples f 180 base pairs. This pattern is nt bserved with chrmatin fixed in urea (Fig. 2 B) which is cnsistent with the bservatins f Carlsn et al. (10). 0.6 c in Ui < m cc t CO B & 10 DISTANCE MIGRATED (CM) 12 Fig. 2. Electrphretic prfile f DNA fragments islated frm a micrcccal nuclease digests f untreated chrmatin (A) and chrmatin fixed with frmaldehyde in the presence f 5 M urea (B). In bth cases the digestins was carried ut t 5% acid sluble prducts. Electrphreais was in 2.5% plyacrylamide gel under nn-denaturing cnditins. 1764

5 Nevertheless, the 10 nucletide repeat survives, as demnstrated in Fig. 3 A. 0.6 ID in a. 0.6 CD < 0.4 B DISTANCE MIGRATED (CM) 12 Fig. 3. DNA fragments frm chrmatin fixed with frmaldehyde in the presence f 5 M urea and digested with DNA.se I t 16.2$ acid sluble prducts (A) and frm chrmatin, digested with DNAee I in the presence f 5 M urea t 18.7# acid sluble prducts. 7.5% plyacrylamide gels, denaturing cnditins. While this study was in prgress, Jacksn and Chalkley (12) reprted that micrcccal nuclease was active in the presence f 5 M urea. This stimulated us t test the activity f DNAse I under the same cnditins. It was fund that the enzyme was 1765

6 active and exhibited its nrmal requirement fr Mg ++, but its specific activity was abut 20 times lwer. Incubatin f chrmatin with DNAse I in the presence f 5 M urea resulted in the nrmal digestin pattern (Fig. 3 B), shwing the 10 nucletide repeat. The persistence f the 10 nucletide repeat in chrmatin fixed in the presence f urea r digested in urea may mean that either this type f peridicity is nt dependent n the secndary flding f the dexynucleprtein fiber (if we assume that urea causes a cmplete unflding) and in this case it is determined by the direct interactins between histnes and DNA, r urea des nt extend the chrmatin cmpletely and sme secndary structural features remain intact t determine the bserved specificity f DNA fragmentatin with DNAse I. The latter pssibility is suggested by the finding f Jacksn and Chalkley (persnal cmmunicatin), that ne can bserve a specific cleavage f chrmatin DNA with micrcccal nuclease in the presence f 5 M urea int apprximately 200 base pairs and multiples. Our results, hwever, definitely pint ut that the 10 nucletide repeat may exist independently f the 180 base pair repeat in the sense that they are determined by different structural parameters f chrmatin. REFERENCES 1 Nll, M. (1974) Nature 251, Van Hlde, K. E., Shaw, B. R., Lhr, D., Herman, T. M. and Kvacic, R. T. (1975) Prceedings f the 10th FEBS Meeting 34, 57-72, Paris 3 Nll, M., Thmas, J. 0. and Krnberg, R. D. (1975) Science 187, Yaneva, M. and Dessev, G. (1976) Eur. J. Bichem. in press 5 Nll, M. (1974) Nucleic Acid Res. 1, laneva, M., Mladenva, J. and Dessev, G. (1976) Anal. Bichem., submitted 7 Sllner-Webb, B. and Felsenfeld, G. (1975) Bichemistry 14, Axel, R. (1975) Bichemistry 14, Bartley, J. A. and Chalkley, R. (1973) Bichemistry 12,

7 10 Duglas Carlsn, R., Olins, A. L. and Olins, D. E. (1975) Bichemistry 14, Panyim, S. and Chalkley, R. (1969) Arch. Bichem. Biphys. 130, Jacksn, V. and Chalkley, R. (1975) Bichem. Biphys. Res. Cmm. 67,

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