Sensitive Assay Detects Protein Methylesterase in Spermatozoa: Decrease in Enzyme Activity During Epididymal Maturation
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1 BOLOGY OF REPRODUCTON 3, (1984) Sensitive Assy Detects Protein Methylesterse in Spermtoo: Decrese in Enyme Activity During Epididyml Mturtion CLAUDE GAGNON, 2 DANELLE HARBOUR,2 EVE DE LAMRANDE,2 C. WAYNE BARDN3 nd JEAN-LOUS DACHEUX4 Unite de Bior#{233}gultion cellulire et mowculire2 Le Centre hospitlier de l Universite Lvl Sinte-Foy, Qulbec, Cnd G V 4G2 nd D#{234} prtement de Phrmcologie et Toxicologie Fculti de M#{233}decine, Universit#{233} Lvl Quibec, Cnd GK 7P4 The Popultion Council3 New York, New York 121 nd CNRS, Fculti des Sciences4 Tours 372 Frnce ABSTRACT A more sensitive ssy for protein methylesterse (PME) ws developed. The new ssy mesures the methnol formed from hydrolysis of protein-methyl esters insted of methyl esters remining on proteins. The formtion of methnol is liner with time nd enyme concentrtion up to 2% of substrte hydrolysis. With this ssy, we hve detected very low PME ctivity in rt spermtoo from cud epididymidis. However, PME ctivity in spermtoo from cput epididymidis ws 1-fold higher. n more detiled study on bull spermtoo during epididyml mturtion, we observed tht PME ctivity ws low in testiculr spermtoo, incresed in spermtoo from cput epididymidis to mximum of 1.29 pmol/mg protein, nd progressively decresed to very low level (.6 pmol/mg protein) in spermtoo from cud epididymidis. The drop in PME ctivity during epididyml trnsit prllels the progressive cquisition of motility nd fertiliing cpcity by spermtoo. NTRODUCTON Protein-crboxyl methylse (PCM) esterifies free crboxyl groups of protein, thus neutrliing negtive chrges on protein substrtes (for review, see Pik nd Kim, 198). The enyme protein methylesterse (PME) hydrolyes methyl ester bonds to yield methnol nd the protein under its originl form before methyltion by PCM (Stock et l., 1978; Ggnon, 1979). PCM nd PME re prts of the protein-crboxyl methylting-demethylting system tht posttrnsltionlly nd reversibly modifies protein chrges, structure nd function Accepted Jnury 24, Received November 7, Reprint requests: Docteur Clude Ggnon, Unite de Bioregultion cellulire et moleculire, C.H.U.L., 275, boul. Lurier, Locl 976, Sinte-Foy (Quebec) Cnd, G1V 4G2. (Ggnon nd Heisler, 1979; Springer et l., 1979; Pik nd Kim, 198; O De et l., 1981; Diliberto, 1982). Wheres PCM ws discovered more thn 1 yers go, PME ws discovered only recently. Since bcteril protein-methyl esters hve long hlf-lives, the enyme PME ws first reported in prokryotes (Stock et l., 1978; Toews et l., 1979). The need for PME in mmmlin cells ws questioned for severl yers s their proteinmethyl esters spontneously hydrolyed within 3 mm under physiologicl conditions (Kim nd Pik, 1976; Ggnon et l., 1978). The possible importnce of PME ws suggested by the recent finding tht the ctivity of this enyme vried more thn 1-fold in rt tissues (Ggnon, 1979). n previous study, we reported tht PME ws present in rbbit ejculted spermtoo but undetectble in rt spermtoo from cud epididymidis (Bouchrd et l., 198). To clrify these seemingly contrdictory results, we reinvestigted the 953
2 954 GAGNON ET AL. PME ctivity in spermtoo using more sensitive nd more ccurte ssy. With this ssy, we were ble to detect PME ctivity in rt spermtoo. n ddition, we report how the ctivity of this enyme chnges in bull spermtoo from different portions of the reproductive Mterils trct. MATERALS AND METHODS S-denosyl-(3 H-methyl)-methionine, 15 Ci/mmol, nd ACS were purchsed from Amershm Corp. (Okville, Ont.), S-denosylhomocysteine from Boehringer-Mnnheim (Montrel, Que.), Sephdex G-25 from Phrmci Fine Chemicls (Montrel, Que.), nd ovlbumin from Sigm Chemicls (St. Louis, MO). PCM ws purified from red blood cells ccording to previously described method (Ggnon, 1979) nd kidney PME by method to be described elsewhere. Collection of Rt Spermtoo Spermtoo from rt cput nd cud epididymides were obtined by mincing these tissues in Gey s medium (1mM NC, 4,7 mm KC, 2.52mM CCl2, 1.13 mm KH2PO4, 2.4 mm MgSO4, 1 mm pyruvic cid, 1 mm sodium lctte, 11 mm glucose, 1 mm Hepes, 15 mm NHCO3) djusted to ph 7.9. Sperm suspensions were filtered through cheesecloth to remove epididyml frgments nd centrifuged t 8 X g for 5 mm. Pelleted spermtoo were resuspended in Gey s medium. Testiculr spermtoo were collected from the rete testis 24 h fter ligtion of the efferent ductules. sodium cette buffer, ph Protein-(3 H-methyl esters were seprted from remining S-denosyl- (3 H-methyl )-methionine by chromtogrphy on Sephdcx G-25 equilibrted in.25 M sodium cette, ph 4.35, contining 5% glycerol nd.1 mm dithiothreitol (PME buffer). Before ppliction on the Sephdex column (1 cm X 17 cm), 2 mg of cytochrome c ws dded to the smple to serve s visul mrker for the position of proteins in the void volume. After chromtogrphy, the protein pek ws collected nd proteinl H-methyl esters were distributed in liquots of 5 M in polypropylene tubes kept on ice to which PME smples or boiled PME smples were dded. After -4 mm of incubtion, the rection ws stopped by the ddition of.1 ml of 15% trichlorcetic cid (TCA) followed by 3 ml of toluene-isomyl lcohol (3:2 by volume). Tubes were cpped, vigorously gitted for 3 see, centrifuged t 5 X g for 1 mm nd the orgnic phse ws collected. One ml ws dded directly to 1 ml of ACS. Another 1-m liquot ws evported to dryness t 6#{176}Cinto scintilltion vil, nd then 1 ml of toluene-isomyl lcohol nd 1 ml of ACS were dded. The rdioctivity in both vils ws counted in liquid scintilltion spectrometer. The difference between the two vils represents the rdioctive methnol produced during the incubtion (Ggnon, 1979), n generl, the nonvoltile rdioctivity represented less thn.2% of the voltile rdioctivity. Protein Determintion Protein concentrtions were determined by the method of Lowry et l. (1951), using bovine serum lbumin s the stndrd. Collection of Bull Spermtoo Bull testes nd epididymides were collected from locl slughterhouse nd immeditely trnsported to the lbortory. Testiculr spermtoo were collected directly from the rete testis nd epididyml spermtoo were obtined from the epididyml duct by perfusion. Spermtoo from cud epididymides were extruded with oil, wheres spermtoo from cput nd corpus epididymides were extruded with Gey s medium by method dpted by Dcheux (198). Sperm suspensions were wshed by centrifugtion (8 X g for 5 mm) with Gey s medium nd resuspended in.25 M sodium cette ph 4.35 contining 5% glycerol nd.1 mm dithiothreitol. Old PME Assy The old PME ssy hs been described in detil elsewhere (Ggnon, 1979). New PME Assy PME ctivity ws determined t 37#{176}Cby sequence of two enymtic rections. Methyltion rection:.4 ml of dilyed ovlbumin (5 mg/m) ws incubted with.4 ml of.25 M sodium cette buffer ph 6.,.4 ml of purified PCM (.1 mg/ml), nd.4 ml of 8 M S-densyl-(3 H-methyl)-methionine (15 Ci/mmol, 125 MCiml). After 3-mm incubtion, the rection ws stopped by the ddition of.4 ml of 1 mm S-denosylhomocysteine (n inhibitor of PCM) in 1 M RESULTS Vlidtion of the New PME Assy When enymticlly synthesied ovlbumin- [3H]-methyl esters were incubted with PME, rdioctive methnol nd unlbeled ovlbumin were formed. The rdioctive methnol produced, incresed linerly between nd 3 mm nd the protein-[3 H-methyl esters remining decresed linerly up to 3 mm (Fig. 1). After 3 mm of incubtion, 22% of the rdioctivity of the originl protein-3 H] -methyl esters were found s [3H] -methyl, wheres 79% of protein- [3H] -methyl esters remined unhydrolyed. These results indicted tht hydrolyed protein [3H] -methyl esters were quntittively recovered s [3H] methnol with the new cid extrction. Similr results were obtined when protein-3 H] -methyl esters were incubted for 2 mm with incresing concentrtions of PME. As in the previous cse, the hydrolysis of protein- [3 H] -methyl esters ws liner between % nd 2% of methyl esters degrded nd the rte of hydrolysis decresed therefter (Fig. 2).
3 PROTEN METHYLESTERASE DURNG SPERM MATU RATON 955. b 2 TME (m,n) FG. 1. Effect of time on the hydrolysis of protein- 3 H -methyl esters. Enymticlly synthesied ovlbummn-[3hl -methyl esters (49, cpm) were incubted with 2.tg of PME. After vrious periods of time (-4 mm), the rdioctive methnol produced during the incubtion ws extrcted under cidic conditions nd counted (for more detils, see the New PME Assy section in Mterils nd Methods). The remining protein-3 H) -methyl esters were determined by lkliniing the cidic queous phse to ph 11 with NOH to hydrolye remining ester bonds nd by extrcting nd counting the chemiclly formed rdioctive methnol. Control incubtions contining no PME or boiled PME showed no significnt degrdtion of protein- (3 H -methyl esters. (.-- -.) Rdioctive methnol enymticlly formed during the incubtion (s-.) Protein-[3 H -methyl esters remining t the end of incubtion. - w U. -J - obtined by subtrcting the 3 H] methnol formed t the end of incubtion ( high vlue) from the [3H]methnol t Time ( very low vlue) (Tble 2). With this ssy, stndrd devitions rnged from 2% to 8% of the men vlue, t hs to be noted tht from the sme mount of protein [3H]-methyl esters incubted, the new ssy gve higher rte of hydrolysis. This difference is due to the fct tht not ll protein-3 H] methyl esters precipitted with TCA. The hydrolysis of the nonprecipitble protein-3 H-methyl esters ws not detected by the old ssy wheres the [3 Hmethnol formed from the hydrolysis of both precipitble nd nonprecipitble protein-3 H]- methyl esters ws detected with the new ssy conditions. Levels of PME Activity in Rt Spermtoo The level of PME ctivity in rt spermtoo ws determined using the new enymtic ssy. The level of PME ctivity ws very low in spermtoo from testes nd cud epididymides (Tble 3). These levels, t the limit of sensitivity of the new ssy, would not hve been detected by the old PME ssy s reported Comprison Between the New nd the Old PME Assy A typicl comprison between the new nd the old ssy is described in Tbles 1 nd 2. n these tbles, only the second rection (PME rection) of ech ssy ws compred. With the old ssy conditions, protein-3 H] -methyl esters remining t the end of the incubtion decresed s the time of contct with PME incresed (Tble 1). With this ssy, the net hydrolysis of protein-3 H-methyl esters ws obtined by subtrcting the protein-3 H]- methyl esters remining t the end of incubtion ( high vlue) from protein-3 H] -methyl esters t Time ( higher vlue). The stndrd devition for ech time point ws especilly high (79% nd 47% of men vlues for Times 5 nd 1, respectively) t erly time points. On the other hnd, with the new ssy conditions, the blnk vlue ws much lower nd the net hydrolysis of protein-3 H] -methyl esters ws tion. - (5 ( Ui - ) -s - LU w PME FG. 2. Effect of enyme concentrtion on the hydrolysis of protein-3 H -methyl esters. Similr conditions s those described in Fig. 1 were used with the exception tht PME concentrtion ws vried from.5 to 5 Mg/ssy nd the incubtion time ws fixed to 2 mm. (..---.) Rdioctive methnol enymticlly formed during the incubtion. (.-.) Protein- 3 H -methyl esters remining t the end of incub- / (M9) / t LU. - U-. Ui
4 956 GAGNON ET AL. TABLE 1. Degrdtion of protein- 3 H-methyl esters by PME using the old ssy conditions. Time Protein-j3 H-methyl esters remining Protein-(3 H-methyl esters hydrolyed ± ± ± ± ± 485 5Protein-Hl-methyl esters (1771 cpm) were incubted with purified protein methylesterse t ph At the end of the vrious incubtion periods, the remining protein-3 H-methyl esters were precipitted with 15% TCA. Precipitted proteins were centrifuged t 1, X g for 1 mm nd the pellet ws resuspended in 2 M of 1 M sodium borte buffer, ph 11.. The rdioctive methnol generted from the lkline hydrolysis ws extrcted nd counted s described elsewhere (Ggnon, 1979). Results re expressed s cpm of protein-3 Hmethyl esters remining (men of triplictes) nd cpm of protein-3 H-methyl esters hydrolyed (men t SD of triplictes). previously (Bouchrd et l., 198). On the other hnd, the PME level ws 8-fold higher in spermtoo from cput epididymidis. Levels of PME Activity in Bull Spermtoo The high nd low levels of sperm PME in cput nd cud epididymides prompted us to investigte in more detils PME ctivity in spermtoo t different stges of mturtion, Becuse bull testiculr spermtoo re redily vilble without ligtion or microsurgery nd TABLE 2. Degrdtion of protein-3 H-methyl esters by PME using the new ssy conditions. Time l H Methnol formed Protein-3 H -methyl esters hydrolyed ± ± ± ± ± 175 proteinl3 H-methyl esters (1771 CPM) were incubted with purified protein methylesterse t ph At the end of the vrious incubtion periods, the enymticlly formed rdioctive methnol ws extrcted t cid ph nd counted s described in Mterils nd Methods. Results re expressed s cpm of H Methnol formed (men of triplictes) nd cpm of protein-3 H-methyl esters hydrolyed (men ± SD of triplictes). becuse epididymides cn esily be divided in 1 segments (Fig. 3), this species ws selected for the mturtion study. PME ctivity ws reltively low (.29 pmol/mg protein) in testiculr spermtoo but it significntly incresed in spermtoo from cput epididymidis, with the mximum level being observed in Segment 3 (1.29 pmol/mg protein) (Fig. 4). PME levels progressively declined s spermtoo reched the corpus epididymidis nd lmost completely disppered when they reched the cud epididymidis. The enyme ctivity in spermtoo from cud epididymidis represented only 4.7% of tht present in spermtoo from Segment 3. DSCUSSON n this report, new ssy conditions for mesuring the degrdtion of protein-methyl esters were described. With this new ssy, the rte of hydrolysis ws liner with respect to time nd enyme concentrtion between % nd 2% of protein-methyl esters hydrolyed. Both the new nd the old ssy detected the degrdtion of protein- H-methyl esters synthesied by incubting PCM nd S-denosyl- (3 H-methyl)-methionine with ovlbumin; however, the new ssy ws more sensitive. For the sme mount of protein-3 H] -methyl esters s substrte, the new ssy gve higher rte of hydrolysis (Tble 1). This ws due to the fct tht some protein-3 H] -methyl esters were not precipitted by the TCA used in the old ssy. The fct tht the new ssy hd low blnk (control, no hydrolysis of methyl esters)
5 PROTEN METHYLESTERASE DURNG SPERM MATURATON 957 TABLE 3. PME ctivity in rt spermtoo from testes, cput nd cud epididymmdes. Sperm origin PME (pmol/mg) ctivity protein) Testis.4 ±.2 (5) Cput epididymidis.34 ±.18 (5) Cud epididymidis.3 ±.1 (7) Sperm suspensions (2 g protein) were incubted decresed progressively to very low level when spermtoo reched the cud epididymidis. This low level of PME ctivity in spermtoo from cud epididymidis ws probbly not due to the presence of n inhibitor within the preprtion since mixing experiments involving spermtoo from Segments 3 nd 1 of the epididymis did not provide ny evidence for such n inhibitor (dt not shown). in the presence of.2% Triton X-1. PME ctivity is expressed in pmol of ovlbumin-methyl esters hydrolyed per mg protein per 2 mm. Vlues represent the men ± SEM of 5 to 7 experiments. vlue in contrst to the high (mximl) vlue of the old ssy ws lso cuse for the improved sensitivity. With the new ssy, hydrolysis generting 2-3 cpm of rdioctive methnol cn be esily detected since controls re round 2-25 cpm. n the cse of the old ssy, significnt nd relible ctivity cn generlly be detected following hydrolysis of bout 1% of substrtes, wheres the new ssy will detect hydrolysis of 1% with better relibility. Another dvntge of the new procedure is the elimintion of protese interference. With the old ssy conditions, the ction of proteses on protein-3 H] -methyl esters would result in the formtion of smller rdioctive-methylted peptides. f these methylted peptides were smll enough not to be precipitted by TCA, their disppernce in the TCA pellet would mimic the hydrolysis of protein-3 H-methyl esters since the old ssy uses the loss of precipitble 13H1 -methyl esters s mesure of PME ctivity. Since only the rdioctive methnol formtion is mesured with the new ssy conditions, interference by proteses is eliminted. With the new PME ssy, we were ble to detect very low levels of ctivity in rt spermtoo from cud epididymidis. These levels were t the limit of relible detection. This explins why, in previous study, PME ws not detected by the old PME ssy (Bouchrd et l., 198). PME ctivity ws 1-fold higher in spermtoo from cput epididymidis. These results were confirmed in more detiled study on epididyml mturtion of bull spermtoo. PME ctivity ws low in testiculr spermtoo but mrkedly incresed in spermtoo from Segment 3 of epididymis. Then, PME ctivity FG. 3. Bull epididymis divided in 1 segments. Spermtoo were collected by perfusion with oil for Segment 1 nd with Gey s medium for ll other segments.
6 958 GAGNON ET AL. of Helth, grnt HD The excellent secretril ssistnce of J. Roy is grtefully cknowledged. REFERENCES TESTS SEG#2 SEG#3 SEG#4 SEG#6 SEG#1O FG. 4. PME ctivity in bull spermtoo from testiculr nd epididyml origin. Spermtoo were collected s described in Mterils nd Methods nd ssyed the sme dy. Sperm suspensions (2 g protein) were incubted in the presence of.2% Triton X-1. PME ctivity is expressed in pmol of ovlbumin methyl esters hydrolyed per mg protein per 2 mm. The height of brs represents the men ± SEM nd the number of experiments is shown in prentheses. Most significnt chnges reported during epididyml trnsit delt minly with membrne components on sperm surfce (Olson nd Hmilton, 1978; Jones et l., 1981) nd little is known bout the chnges in mcromolecules inside spermtoo. n previous study, we hve reported tht sperm PCM nd methyl cceptor proteins mrginlly vried when rt sperm trnsit from cput nd cud epididymidis (Bouchrd et l., 198). n similr study, Purvis et l. (1982) observed tht the level of PCM ctivity in spermtoo incresed 3-fold from the first segment of the cput to the very lst segment of the cud epididymidis. These results nd those from the present study indicte tht within the protein-crboxyl methylting-demethylting system, the enyme PME is the most ffected during cquisition of sperm motility nd/or cpcity to fertilie. Nevertheless, s this system posttrnsltionlly nd reversibly modifies the chrge, structure nd function of proteins, ny chnge in ny of its components will ffect the net number of protein-methyl esters, which is the physiologiclly importnt prmeter. The chnges in sperm components of the methylting system during epididyml trnsit should result in much higher number of proteins with methyl esters in spermtoo from cud epididymidis s compred to tht in spermtoo from cput epididymidis. ACKNOWLEDOMENTS This reserch ws supported in prt by the Medicl Reserch Council of Cnd nd the Ntionl nstitute Bouchrd, P., Ggnon, C., Phillips, D. M. nd Brdin, C. W. (198). The loclition of protein-crboxyl methylse in sperm tils. J. Cell Biol. 86: Dcheux, J. L. (198). An in vitro perfusion technique to study epididyml secretion. RCS (nt. Res. Commun. Syst.) Med. Sci. Libr. Compend. 8:137. Diliberto, E. J., Jr. (1982). Protein-crboxyl methyltion: Puttive role in exocytosis nd in the cellulr regultion of secretion nd chemotxis. n: Cellulr Regultion of Secretion nd Relese (P. M. Conn, ed.). Acdmic Press, New York, pp Ggnon, C. (1979). Presence of protein methylesterse in mmmlin tissues. Biochem. Biophys. Res. Commun. 88: Ggnon, C. nd Heisler, S. (1979). Protein crboxylmethyltion: Role in exocytosis nd chemotxis. Life Sci. 25: Ggnon, C., Viveros,. H., Diliberto, E. J., Jr. nd Axelrod, J. (1978). Enymtic methyltion of crboxyl groups of chromffin grnule membrne proteins. J. Biol. Chem. 253: Jones, R., Pholprmool, C., Setchell, B. P. nd Brown, C. R. (1981). Lbeling of membrne glycoproteins on rt spermtoo collected from different regions of the epididymis. Biochem. J. 2: Kim, S. nd Pik, W. K. (1976). Lbile protein-methyl esters: Comprison between chemiclly nd enymticlly synthesied. Experienti 32: Lowry,. H., Rosenbrough, N. J., Frr, A. L. nd Rndll, R. J. (1951). Protein mesurement with the Folin phenol regent. J. Biol. Chem. 193: O De, R. F., Viveros,. H. nd Diliberto, E. J. Jr. (1981). Protein crboxylmethyltion: Role in the regultion of cell functions. Biochem. Phrmcol. 3: Olson, G. E. nd Hmilton, D. W. (1978). Chrcterition of the surfce glycoproteins of rt spermtoo. Biol. Reprod. 19: Pik, W. K. nd Kim, S. K. (198). Protein Methyltion. John Wiley & Sons, New York. Purvis, K., Cusn, L., Attrmdl, H., Ege, A. nd Hnsson, V. (1982). Rt sperm enymes during epididyml trnsit. J. Reprod. Fertil. 65: Springer, M. S., Goy, M. F. nd Adler, J. (1979). Protein methyltion in behviourl control mechnisms nd in signl trnsduction. Nture 28: Stock, J. B nd Koshlnd, D. E., Jr. (1978). A protein methylesterse involved in bcteril sensing. Proc. Nt. Acd. Sci. USA 75: Toews, M. L. nd Adler, J. (1979). Methnol formtion in vivo from methylted chemotxis proteins in Escherichi coli. J. Biol. Chem. 254:
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