BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS
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1 HYPOGLYCEMIC ACTION OF 2-AMINONORBORNANE-2-CARBOXYLIC ACID IN THE RAT* H. S. Tager and H. N. Christensen Department f Bilgical Chemistry, The University f Michigan Ann Arbr, Michigan Received May 19, 1971 SUMMARY: Crrect rientatin f the amin and carbxyl grups and f the bicyclic ring f the cmpund 2-aminnrbrnane-2-carbxylic acid is essential fr its inductin f a tlbutamide-ptentiated hypglycemia in the rat, an effect which we have already shwnt arise frm stimulatin f insulin release. Only that ismer with its carbxyl grup ~x and the abslute cnfiguratin 12, 2S, 4S has this actin. This finding prvides a partial descriptin f a recgnitin site whereby neutral amin acids stimulate insulin release. A partially purified preparatin f the nn-metablizable amin acid 2-aminnrbrnane-2-carbxylic acid (BCH) ~ prduces a tlbutamide-ptentiated hypglycemia in the rat which has been shwn t be assciated with increases in the immun!gically-reactive insulin f the plasma 3. Using a preparatin f BCH enriched in ne f the gemetric ismers which we call (±)b 4, Fajans et a~. 5 shwed that the insulin-releasing actin f this cmpund in the dg resembles that f leucine and differs frm that f arginine and lysine in fur significant aspects. BCH prved als t be a valuable mdel substrate fr + transprt, reacting with principal Na -independent systems in several animal 4,6 cells and tissues, and with a system fr branched-chain amin acids in E. cli 4. We have nw islated the fur ismers f BCH (Table I) and are re- prting here the sterespecificity f their hypglycemic actin in the rat. Supprted in part by grant HD frm Natinal Institutes fr Child Health and Human Develpment, Natinal Institutes f Health, U.S.P.H.S. H.S.T. received supprt frm N.I.H. Training Grant Preliminary reprts f these studies have appeared I'2. TThe abbreviatin used is BCH, 2-aminnrbrnane-2-carbxylic acid. 185
2 VI. 44, N. 1, 1971 EXPERIMENTAL The gemetric ismers f BCH were prepared by in-exchange chrmatgraphy f the mixtures synthesized by either the Bucherer r the Strecker prcedure 4'7. The racemic pairs, called a and b (r fr greater precisin, (±)a and (±~b), were then reslved as the brucine salts f the N-frmyl amin acids 8. The abslute cnfiguratins f the fur ismers have been identified 8,9 by physical, chemical and bichemical techniques The Sprague-Dawley rats used were 50 t i00 g males which were first treated with 20 mmles/kg f tlbutemide injected intraperitneally every 12 hr fr 48 hr (5 dses). The animals were fasted 20 hr, and the amin acid then injected 2 hr after the last dse f tlbutamide. A sample f fasting bld was cllected frm the tail, and the test amin acid injected intra- peritneally in a slutin cntaining enugh NaCl t make it isssmlar with bld plasma. Further bld samples were taken at the intervals shwn in the figures, and their cntent f glucse was measured using an ultramicr adap- tatin f the glucse xidase assay I0 with the enzyme preparatin Gludstat f the Wrthingtn Bichemical C. The decline in the levels fr a given interval was calculated by reference t crrespnding results with tw cntrl rats simultaneusly receiving nly NaCl slutin. RESULTS Figure i cmpares the hypglycemic activity f the tw racemic mixtures (±)a and (±)b, and indicates that nly the BCH preparatin with the carbxyl grup 8x (the b frm) is effective in lwering the bld glucse in tlbuta- mide-primed animals. Althugh the hypglycemic actin f (±),b-bch appears t be bth mre prlnged and mre severe than that f ~-leucine, in the dg in cntrast the hyperinsulinemic actin f BCH is neither as prlnged nr as severe as that f L-leucine 5. = Since the precursr was racemic nrbrnanne, each preparatin f the gemetric ismers (a and b) must necessarily be cmpsed f tw ptical is- 186
3 nq <~ I ] I } Time, hr Fig. i. Hypglycemic actin f the gemetric ismers f BCH. The racemic mixtures were injected intraperitneally at a dse f 8 mmles/kg int fasted, tlbutamide-primed ra~s as described. The rdinate recrds the change in bld glucse levels by reference t saline-injected cntrls. The vertical bars represent duplicate experimental animals. The effect f leucine is shwn fr reference. Table I. Assignment f strutures fr the fur ismers f BCH. The assignments are summarized frm reference 8. 7 Substituent at psitin Ismer 5 " 4 designatin A B C 3 A (-)-a-bch H H NH~ D c~ (+)-a-bch NH~ CO X H 6 (-)-b-bch H H CO X H NH~ O + H (+) -b-bch C02 NH 3 I-t mers, as shwn in Table I. Fig. 2 demnstrates that f the ptical ismers present in (±)b, nly the levrtatry frm has measurable hypglycemic acti- vity. Therefre the dse f bilgically active BCH used in the studies f Fig. 1 was really nly half that recrded in the legend. Fig. 3 measures the maximally effective dse f (±)-b-bch under the cnditins used, and shws that, at lw levels, the effective dse f (-)-b-bch n a mlar basis is half that f the racemic mixture, indicating that n inhibitin is exerted by (+) -b-bch. 187
4 BIOCHEMICAL AND BIOPHYSICAl. RESEARCH COMMUNICATIONS "~ -i E -20 -~ \ I I I I Time, hr Hypglycemic actin f the ptical ismers f b-bgh. Fig mmles/kg, the animals being treated as in Fig. i. The dse was O _ E a -30 -~ -I0 O O ~ / (-)-b-sch / (+)- b-bch m r I ; I 5 I Dse, mrnles / kg Dse-effect relatins fr (±)-b-bch and (-)-b-bch in causing hyp- Fig. 3. glycemia. The animals were handled as in Fig. i. The pints pltted are fr results 1 hr after administratin f the amin acids. The dashed arrws shw, when we administered purified (-)-b-bch, hw much (±)-b-bch wuld have supplied the same amunt f the effective ismer. Of several ther analgs f BCH and leucine tested fr their ptential hypglycemic activity, ~-isleucine decreased the bld glucse cncentratin nly abut half as much as did ~-leucine, whereas the amin acids 1-amin- cyclpentanecarbxylic acid, its 3-methyl derivative, the racemic ~-cycl- pentane derivatives f glycine, alanine and s-amin-n-butyric acid, the racemic ~-methyl-~-cyclpentane derivatives f glycine and alanine, als ~- valine, L-nrleucine and D-leucine were ineffective under the cnditins used. = = 1 RR
5 2-Methyl-l-amincyclpentanecarbxylic acid decreased the bld glucse level t a very small extent. In a single experiment by S. S. Fajans and S. Pek, intravenus infusin during 15 min f 16 mmles f (±)-b-bch int a 4-kg female dg failed t cause a significant increase in the plasma insulin within an interval f 2 hr. DISCUSSION Because f the abve differences in the behavir f the ismers f BCH, we were pleased with the prpsal f Prfessr Be Hellman and his assciates at the University f Umea that the actin f this amin acid be studied in micrdissected pancreatic islets frm an bese, diabetic strain f mice. Again fr this preparatin, nly the levrtatry frm f the b ismer prved effective in stimulating insulin secretin, althugh transprt studies shwed that bth (-)-b-bch and (+)-b-bch were cncentrated by this tissue ll. One f its advantages is that this preparatin can be expsed t any cncentratin we chse f an amin acid. Quite pssibly, a partial effectiveness f sme f the amin acids tested fr hypglycemic r insulin-releasing 4'5 actin may have been bscured by the difficulty f bringing them t high enugh levels in the living animal. In all ther tissues studied in islatin, including segments f ham- ster intestine, the Ehrlich ascites tumr cell, the pigen erythrcyte and E. 00~ K-12, we find that the (-)b ismer is transprted mre rapidly than its enantimrph, and where tested, with greater apparent affinity. The dis- tributins f the enantimrphs in the intact rat prved, hwever, rather similar 12. Reactivity f neutral amin acids with a recgnitin site fr stimulating the secretin f insulin is apparently cnditined by the fllwing structural features: (i) The sidechain shuld have cnsiderable aplar bulk, which can be prvided by branching r ring frmatin; (2) this bulk shuld be distributed t crrespnd t an amin acid in its ~ cnfiguratin; and 189
6 (3) a branch n the alpha carbn with the cnsequent absence f an alpha hydrgen is nt detrimental if ther steric cnsideratins are met. Beynd these features, we may see that certain dispsitins f the mass f the bicyclheptyl ring are unfavrable, and ne dispsitin is favrable. These dispsitins can be t sme degree mimicked by the ismeric leucines. We have pinted ut earlier hw all f the carbn atms f leucine r isleucine might be identified each with a carbn atm f BCH 4. In the case Of L-isleucine the present results d nt disturb whatever validity that placement has in describing a pssible rientatin fr this amin acid at the receptr site. If we picture its carbxyl grup at psitin C in the sketch f Table I, and its amin grup at 0, then carbn atms i, 6 and 5 (r i, 7 and 4) culd represent the principal chain, in which case atms 7 r 6 wuld represent the branching methy I grup. Carbns 3 and 4 f the sketch will be left ver t strut the rientatin taken in BCH. In the case f D-leucine we = can als identify each f its sidechain carbn atms with ne f the numbered atms in the sketch, atms 1 and 6 f the sketch being in that case left ver. But since D-leucine appears inert the site apparently des nt stabilize the = amin acid sufficiently in that r anther suitable rientatin t prduce tight enugh binding at the cncentratins used. Beginning with the same placement f the carbxyl and amin grups f the effective L ismer f leu- cine, we may identify nly 3 f the 4 atms f its sidechain with atms in the sketch, ~.~., with atms i, 7 and 4 r atms i, 6 and 5. The secnd methyl grup f leucine is then left t prject frm atms 6 r 7. We cannt yet say what latitude is acceptable in the placement f a single sidechain carbn atm at the receptr site, because each f these has nt yet been varied independently in a knwn way. All we say is that the bulk represented by the bicyelic ring structure cannt be received effectively if it is shifted a few ~ngstrms tward the bserver, taking the carbxyl and amin grups as pints f reference, nr can it be receive= effectively if the cyclpentane ring 1,6,5,4,7 is turned upside dwn. 190
7 The structural requirements fr the stimulatin f insulin release are remarkably similar t thse fr transprt f the abve test amin acids by E. ~Zi I'4'12. In neither case, hwever, d we prpse that the effect arises frm a simple, static ccupatin f the recgnitin site; that site presumably must first respnd with a significant structural change. Des- criptin f that change calls fr identificatin f cmpetitive inhibitrs that cannt themselves prvke the respnse. Further cmplementary descrip- tin f the bilgical recgnitin sites and the factrs necessary t their respnses shuld be accessible thrugh the test f additinal mdel substrates REFERENCES i. H. S. Tager, H. N. Christensen, A. M. Cullen, S. S. Fajans, H. N. Flyd and R. Zand, Federatin Pra., 28, 574 (1969). 2. H. S. Tager, A. M. Cullen and H. N. Christensen, Federatin P re., 29, 300 (1970). 3. H. N. Christensen and A. M. Cullen, J. Bil. Chem., 244, 1521 (1969). 4. H. N. Christensen, M. E. Handlgten, I. Lam, H. S. Tager and R. Zand, J. Bil. Chem., 244, 1510 (1969). 5. s. s. Fajans, R. Quibrera, S. Pek, J. C. Flyd, Jr., H. N. Christensen and J. W. Cnn, J. Clin. Endcr. Metab., in press fr July H. S. Tager, T.-C. Sha and H. N. Christensen, Federatin Prd., 30, 235 (1971). 7. H. S. Tager and R. Zand, An~l. Bi~hem., 34, 138 (1970). 8. H. S. Tager and H. N. Christensen, manuscript in preparatin. 9. P. Apgar and M. Ludwig, manuscript in preparatin. i0. A. St. G. Huggett and D. A. Nixn, Lancet, 2, 368 (1957). ii. H. N. C.hristensen, B. Hellman, A. Lernmark, J. Sehlin, H. S. Tager and I.-B. Taljedal, Bichim. Biphy8. Aata, in press. 12. H. S. Tager and H. N. Christensen, manuscript in preparatin. 191
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