TIME RESPONSE OF JEJUNAL SUCRASE AND MALTASE ACTIVITY TO A HIGH SUCROSE DIET IN NORMAL MAN

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1 GASTROEKTEROLOGY Copyrght 1969 by The Wllams & Wlkns Co. Vol. 56, No.3 Prnted n U.S.A. TIME RESPONSE OF JEJUNAL SUCRASE AND MALTASE ACTIVITY TO A HIGH SUCROSE DIET IN NORMAL MAN NORTON S. RoSENSWEIG, M.D., AND RoBERT H. HERMAN, M.D. Metabolc Dvson, Unted States Army Medcal Research and Nutrton Laboratory, Ftzsmons General Hosptal, Denver, Colorado Ths study determned the tme requred for the adaptve changes n human jejunal sucrase and maltase actvtes when detary carbohydrate was changed from glucose to sucrose, sucrose to carbohydrate-free, and glucose to fructose. Four volunteer subjects were studed. The tme for the ncreases and decreases n actvty was 2 to 5 days and there was no further change for 9 weeks thereafter. Ths tme response s smlar to the estmated tme for ntestnal epthelal cell turnover n the small ntestne of man. It s proposed that the changes n dsacchardase actvty produced by changes n detary sugar content are due prmarly to an effect on the crypt cell. The effect becomes ncreasngly manfest as these crypt cells dvde and mgrate up the vllus. Recent studes n ths laboratory have demonstrated that detary sucrose, as compared to detary glucose, sgnfcantly ncreases jejunal sucrase and maltase actvtes but not lactase actvty, n man.! Receved July 20, Accepted October 10, Ths work was presented n part at the Natonal Meetng of the Amercan Gastroenterologcal Assocaton to the Gastroenterology Research Forum, May 16, 1968, at Phladelpha, Pennsylvana. Address requests for reprnts to: Captan Norton S. Rosensweg, Unted States Army Medcal Research and Nutrton Laboratory, Ftzsmons General Hosptal, Denver, Colorado We gratefully acknowledge the assstance of Doctor D. Zakm, for helpful dscusson; Major C. Mller and Captan T. Arnold and ther staff for preparaton of the dets; Major P. Forney and her staff for nursng assstance; Mr. R. Coppes for laboratory assstance; Sergeants D. Jacquart and H. Muntz for help n performng the bopses; and Mss L. Carlson for secretaral ad. The volunteer subjects were provded through the cooperaton of Doctor Norman F. Wtt, Professor of Chemstry, Unversty of Colorado, and the Surgeon General, Unted States Army, Contract DA MD 549, as part of the Conscentous Objector program. The provsons of the contract make t oblgatory to obtan nformed consent n In these studes, the sucrose effect was reproduced by detary fructose, but not by detary lactose, maltose, or galactose. Although ths effect was observed to occur n 1 week, the exact tme requred to produce ths change s not known. The present study was undertaken to determne the tme requred for ths adaptve change n jejunal dsacchardase actvty to occur, and to gan some nsght nto the mechansm of ths change. A prelmnary report has appeared n abstract form. 2 Methods Subjects. Four normal male Caucasan volunteers, rangng n age from 19 to 23, wth no hstory of dsaccharde ntolerance, were studed. All studes were conducted on a metabolc ward. Subjects were weghed daly after vodng and before breakfast. Dets. The desgn of the dets was smlar to those descrbed earler. I Except where ndcated, proten was n the form of sodum general for the subject's servces, and specfcally for each defntve study, and precludes the n vvo use of any radoactve substance. 500

2 March 1969 TIME RESPONSE TO A HIGH SUCROSE DIET 501 casenate and fat as corn ol. The composton. of the dets s lsted n table L Dsacchardase assays. Jejunal tssue was obtaned and dsacchardase actvty was assayed as prevously descrbed.' Specfcally, the method of Dahlqvse was used wth the substrates, lactose, sucrose, and maltose, made up n a maleate buffer at ph 5.8. One unt of dsacchardase actvty s equal to 1 /-Imole of substrate hydrolyzed per mn per g wet weght of mucosa. Recent studes 4 have demonstrated that condtons of storage may alter dsacchardase actvty when expressed n unts per gram wet weght of mucosa. Ths s apparently due to a decrease n tssue water durng storage. At the tme of bopsy n our studes, all specmens were cut n two or three equal peces (dependng on the sze of the bopsy). These specmens were wrapped n weghng paper, placed n plastc contaners, capped, mmedately frozen n acetone and Dry Ice, and stored at - 85 C. All specmens were weghed at the tme of assay and were subjected to smlar perods of thaw. The same procedures were followed n all assays and specmens from the dfferent dets n the same ndvdual were assayed on the same day to mnmze techncal and tme of storage varatons. Snce tssue water was not measured, and we have expressed our data n unts per gram wet weght of mucosa, t s theoretcally possble that the condtons of storage and assay have produced the results obtaned. However, reassay of the tssues at varyng ntervals after storage at - 85 C revealed only slght changes n enzyme actvty. These changes are of much lesser magntude than the changes seen wth alteraton of det. Therefore, these slght changes due to storage cannot account for the degree of changes observed n the enzyme actvty due to det. Study TABLE 1. Composton of the dets Det Carbohydrate Fat Proten % cal % cal % cal I Glucose Sucrose II Carbohydrate-free III Glucose Fructose IV Sucrose In addton to expressng the results n unts of actvty, sucrase to lactase (S/L) and maltase to lactase (MIL) ratos were computed for each bopsy. Snce there was no change n lactase actvty on the glucose and sucrose dets, ths method of expressng the data s employed n an attempt to avod some of the varablty of dsacchardase levels due to depth of bopsy that s characterstc of peroral bopsy specmens n humans.,,5 The data, then, are expressed n unts per gram wet weght of mucosa and n ratos. We have arbtrarly termed the unts absolute actvty,' although quanttatve actvty may be a more exact term snce we are not expressng actvty per gram of purfed dsacchardase proten. Ths desgnaton of absolute actvty s used to compare unts of actvty wth the SIL and MIL ratos whch mght be consdered as relatve actvty. Studes. The nvestgatons were dvded nto four studes. In study I, three subjects were fed a 60% carbohydrate lqud det for 17 days. The frst 9 days; the carbohydrate was entrely glucose; the last 8 days, t was entrely sucrose. To study the amount of tme requred for the change n dsacchardase actvty to occur, seral jejunal bopses were performed daly on days 7 through 12 and 15 through 17. Subjects 1 and 2 were fed a carbohydratefree det for 9 days after the 8 days of 60% sucrose n study I. Ths comprsed study II. On the carbohydrate-free det bopses were performed on days 1, 4, and 9 n subject 1 and days 1, 2, 5, and 9 n subject 2. In study III, subject 4 was fed 40% glucose for 8 days and then 40% fructose for 7 days. Bopses were performed on days 1, 3, 5, 8, 10, 12, and 15. In study IV, subjects 1 and 2 were fed 80% sucrose for 9 weeks. Control bopses were obtaned several days before the det was begun and then perodcally throughout the study. In studes I and II the subjects ate a cal lqud det and n studes III and IV, a cal lqud det. In study II, a 2800-cal, carbohydrate-free, part sold and part lqud det of 75% fat and 25% proten was fed. (A lqud det of 75% corn ol and 25% sodum casenate s unpalatable and produces darrhea.) Weghts remaned constant throughout the perod of study. Results A comparson of mean dsacchardase actvtes on glucose and sucrose dets n

3 502 ROSENSWEIG AND HERMAN Vol. 56, No.3 48 DGLUCOSE _SUCROSE >- 32 I- en > 0 I- 6 ;: U <t <I a:: 1>. 4 ~ 16 0 en I Z ::> o LACTASE MALTASE S/L MIL FIG. 1. Mean dsacchardase actvtes and ratos n subjects 1 to 3 on glucose and sucrose dets. The standard error of the mean s n brackets. TABLE 2. Mean dsacchardase values and sucrase DIET -4- GLUCOSE SUCROSE to lactase (S/L) and maltase to lactase (M/L) ratos on glucose, sucrose, and carbohydratefree SUBJECT 1 3 dets I Study Det 1 Day Lac- Su- Maltase S/ L MI L I I tase crase I I Glucose SUBJECT 2 Sucrose I ! ! I FIG. 2. Seral sucrase to lactase (S/L) ratos n subjects 1 to 3 on glucose and sucrose dets. zo 1 II Carbohy drate- 19b free 2lb ', I a Mean of subjects 1 to 3 n study I, subjects 1 and 2 n study II. b Values for subject 2 only. c Values for subject 1 only. study I s presented n fgure 1. (Days 10, 11, and 12 are not ncluded because ths was the perod of transton at the begnnng of the 60% sucrose det). These results are smlar to and confrm those reported earler.' The tme requred for the ncrease n sucrase actvty to occur n each subject s shown n fgure 2. (The data are ex- pressed n SIL ratos to mnmze varablty from depth of bopsy.) There was no change n the SIL ratos on the frst day of sucrose feedng. It rose abruptly on the 2nd day n subject 2, and on the 3rd day n subject 1. Wth subject 3, there was no rse by day 3, and SIL appeared to requre about 4 to 6 days to obtan a rse on sucrose feedng. The mean daly ab-

4 March 1969 TIME RESPONSE TO A HIGH SUCROSE DIET 503 solute actvtes and ratos n studes I and II are gven n table 2. The results for the MIL ratos are very smlar to those wth S/L, both n terms of degree of response and tme requred for the change. The tme course of the S/L ratos n subjects 1 and 2 when ther det was changed from 60% sucrose to carbohydrate-free (study II) s shown n fgure 3. Agan, the tme requred for the change n S/L s about 3 to 5 days. From fgures 2 and 3, t can be seen that the tme requred for both ncreases and decreases n S/L when the det s changed s smlar. The results n study III are shown n fgure 4. The tme response of S/L when the det s changed from 40% glucose to 40% fructose s smlar to the other studes. Study IV demonstrates that the tme response of S/L to changes n the det s complete n about 5 days and then does not change f the same det s mantaned for several weeks (fg. 5). In addtonal studes, not reported here, 2 subjects were fed glucose for 2 months and then DIET - SUCROSE CHO-FREE o SUBJECT! 3 SUBJECT 2 FIG. 3. Seral sucrase to lactase (S/L) ratos n subjects 1 and 2 on sucrose and carbohydrate-free dets. 2.0 GLUCOSE FRUCTOSE 0.5 FIG. 4. Sucrase to lactase (S/L) ratos n subject 4 on glucose and fructose dets S,{ 3 21 I I 0 I CONTROL DAY 5 DAY 19 DAY64 FIG. 5. Mean sucrase to lactase (S/L) ratos n subjects 1 and 2 on a long term 80% sucrose det. sucrose for 1 week. The S/L and MIL ratos remaned constant on the glucose det and ncreased 3 days after the det was changed to sucrose. Ths obvates any delayed responses to carbohydrates as an explanaton for these fndngs. Dscusson These studes confrm our prevous work l that specfc detary sugars can regulate jejunal dsacchardase actvty

5 504 ROSENSWEIG AND HERMAN Vol. 56, No.3 n man and extend the earler observatons by demonstratng that the tme requred for ths regulaton to occur s approxmately 2 to 5 days. In addton, there was no further change n actvty after 5 days, even when 80% sucrose was fed for many weeks. The tme of ncrease n actvty s equal to the tme of decrease n actvty and s ndependent of the order and types of dets. Two ponts should be noted. Frst, there s a unform tme response for each ndvdual to detary change. Second, ths tme response of 2 to 5 days concdes wth the estmated tme for ntestnal cell turnover n the small ntestne of man. 6-9 It should be stressed that the data reported merely measure the tme response resultng from changes n detary sugars and do not n any drect way determne the mechansm for ths change n dsacchardase actvty. However, snce the tme response for the change n dsacchardase actvty s smlar to ntestnal cell turnover tme, t s qute possble that the changes caused by detary alteraton are medated va the crypt cell and ntestnal cell turnover. The concept of regulaton of dsacchardase actvty va the crypt cellmples that dsacchardase actvty, once determned for a gven cell, remans constant throughout the lfe of that cell. Ths concept of enzyme stablty s supported by the work of Lpkn and Quastler. 10 Usng 14C_ and 3H-labeled leucne, they demonstrated stablty of syntheszed proten n rapdly prolferatng crypt epthelal cells and a slow loss of proten from the mature cells as they mgrated up the vllus. Further support of the hypothess for correlaton wth ntestnal cell turnover comes from the work of Dallman. ll Usng hstochemcal studes of ntestnal cytochrome oxdase repar durng the treatment of copperdefcent rats, he demonstrated that the repar starts n the newly dfferentatng cells at the base of the vllus and then progresses toward the tp of the vllus at a rate approxmatng the normal turnover rate of ntestnal mucosa. By employng smultaneous drect measurement of the turnover rate (e.g., wth trtated thymdne) and dsacchardase actvty, one could determne whether the tme response of dsacchardase actvty and the turnover rate were smlar. If ths effect s a reflecton of the rate of ntestnal cell turnover, one would expect the followng n each ndvdual: (a) the tme requred for ncreases and decreases n actvty should be the same; (b) the tme response to dfferent detary sugars should be the same; (c) there should be no further response after approxmately 5 days; and (d) the tme response should change n lke manner f the turnover rate changes. In addton to the above crtera n man, conclusve proof would requre smlar studes n dfferent speces wth dfferng turnover rates. The studes reported here satsfy the frst three of the four crtera lsted above. We suggest the followng hypothess to explan these results. The changes n dsacchardase actvty produced by changes n detary sugar content are due prmarly to an effect on the crypt cells. The effect becomes ncreasngly manfest as these crypt cells wth new nformaton dvde and then mgrate from the crypt up to the tp of the vllus. Further studes should determne whether the above hypothess s true or whether the effect s prmarly at the vllus epthelal cell level wth a delayed appearance. REFERENCES 1. Rosenweg, N. S., and R. H. Herman Control of jejunal sucrase and maltase actvty by detary sucrose or fructose n man. J. Cln. Invest. 47: Rosensweg, N. S., and R. H. Herman Tme response of jejunal sucrase and maltase actvty to a hgh sucrose det (abstr.). Gastroenterology 54: Dahlqvst, A A method for assay of n-

6 March 1969 TIME RESPONSE TO A HIGH SUCROSE DIET 505 testnal dsacchardases. Anal. Bochem. 7: Walter, W. M., and G. M. Gray Enzyme assay of peroral bopses: storage condtons and bass of expresson. Gastroenterology 54: Townley, R. R. W., K. T. Khaw, and H. Schwachman Quanttatve assay of dsacchardase actvtes of small ntestnal mucosal bopsy specmens n nfancy and chldhood. Pedatrcs 36: Bertalanffy, F. D., and K. P. Nagy Mtotc actvty and renewal rate of the epthelal cell of the human duodenum. Acta Anat. 45: Lpkn, M., P. Sherlock, and B. Bell Cell prolferaton knetcs n the gastrontestnal tract of man. II. Cell renewal n stomach, leum, colon, and rectum. Gastroenterology 45: Shorter, R. G., C. G. Moertel, J. L. Ttus, and R. J. Retemeer Cell knetcs n the jejunum and rectum of man. Amer. J. Dg. Ds. 9: MacDonald, W. C., J. S. Trer, and N. B. Everett Cell prolferaton and mgraton n the stomach, duodenum and rectum of man: radoautographc studes. Gastroenterology 46: Lpkn, M., and H. Quastler Studes of proten metabolsm n ntestnal epthelal cells. J. Cln. Invest. 41: Dallman, P. R Cytochrome oxdase repar durng treatment of copper defcency: relaton to mtochondral turnover. J. Cln. Invest. 46:

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